Biodiversity and structure of the polychaete fauna from soft bottoms of Bahia Todos Santos, Baja California, Mexico

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Deep-Sea Research II 51 (2004) 827–847

Biodiversity and structure of the polychaete fauna from soft bottoms of Bahia Todos Santos, Baja California, Mexico V. D!ıaz-Castan˜edaa,*, L.H. Harrisb a b

CICESE, Departamento de Ecolog!ıa, Km 107 Carret, Tijuana-Ensenada, Apdo. Postal 2732, C.P. 22860 Ensenada, Baja, CA, Mexico Natural History Museum of Los Angeles County, Research and Collections, 900 Exposition Boulevard, Los Angeles, CA 90007, USA Received 14 February 2003; accepted 3 May 2004

Abstract This paper describes diversity patterns of the polychaete fauna in Bah!ıa Todos Santos (Pacific Ocean, Baja California, Mexico). Thirty-nine stations were sampled in October 1994. Measurements of depth, temperature, salinity, dissolved oxygen, organic content and sediment particle size were made. Polychaetes constituted 64% of all invertebrate macrofauna, with 13,757 specimens in 44 families representing 203 species. The best represented families were Spionidae, Capitellidae, Paraonidae, Cirratulidae, Maldanidae, Ampharetidae and Nephtyidae. Bah!ıa Todos Santos presented high species richness (species/station); values varied between 6 (near the harbor) and 67 species (next to Estero Punta Banda). Higher species richness values (48 species to 67/station) were located in the southern section of the bay. Abundances (individuals/station) were generally high (120–1434) except for some coastal stations. Nearly onethird of the stations presented H 0 values higher than 4.00. Diversity (H 0 ) values ranged from 2.06 to 4.80; higher diversity values were found in the southern section of the bay. The stress-predictability modeling characterized approximately 70% of stations as presenting favorable and stable conditions. Pearson and Bray–Curtis coefficients separated stations in relation to their sediment particle size, depth and location in the bay. Principal component analysis determined that organic matter content, percentage of silt-clay, and water depth accounted for 95% of the total variance for all environmental factors measured. Correspondence analysis distinguished three groups of species: Group A species with an extensive distribution throughout the bay and relatively high abundances, Group B species abundant in the shallow areas, especially near the harbor, and Group C species present in the area of the submarine canyon. Non-metric multidimensional scaling analysis separated five groups of stations, depending on depth, grain size and location in the bay. Our results show that Bah!ıa Todos Santos is a favorable environment for polychaete development, their distribution being strongly related to sediment characteristics. The dominant trophic group corresponds to deposit-feeders (91 species). r 2004 Elsevier Ltd. All rights reserved.

1. Introduction *Corresponding author. Tel.: +52-6461750500X24241; fax: +52-6461750545. E-mail address: [email protected] (V. D!ıaz-Castan˜eda).

The organisms that reside in marine sediments constitute the largest faunal assemblage on Earth in areal coverage. The biomass in these sediments

0967-0645/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2004.05.007

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is dominated by macrofauna, particularly by polychaetes. Macrofaunal activity impacts global carbon, nitrogen and sulfur cycling, transport, burial and metabolism of pollutants, secondary production including commercial species, and transport of sediments (Snelgrove, 1998). Coastal marine benthic communities are threatened by human activities, and the present rate of habitat degradation is alarming (Gray, 1997). It is therefore important to improve our understanding of macrobenthos biodiversity in marine sediments. Although studies have been done on the community composition and distribution of sublittoral benthic ecosystems along the Baja California coast (Mun˜oz Palacios, 1993; Pe! rez Pen˜a, 1994), the northern portion of the Mexican Pacific coast remains largely unknown with regard to its polychaete fauna. Bah!ıa Todos Santos is an important bay located in the Pacific coast, in front of the city of Ensenada, and is subjected to industrial and domestic pollution (San˜udo-Wilhelmy et al., 1985). The discharges have increased in the last two decades through rapid human and industrial growth. Few papers have dealt with polychaetes in this region. Liza! rraga-Partida (1974) used polychaetes as indicators of the pollution level, but the area studied was limited to Ensenada harbor. Encalada-Fleitez and Milla! n! ˜ ez (1990) studied molluscs, crustaceans, echiNun noderms and polychaetes in 14 stations located only along the 10 m isobath. Rodr!ıguez-Villanueva et al. (2000) analyzed polychaete family composition in approximately 35 stations distributed throughout the bay. The present study includes all soft-bottom areas of the bay, with the exception of the harbor (7% of the total area). The purpose of this paper was to study polychaete diversity and organization in Bah!ıa Todos Santos. This is the first paper that deals with the polychaete community at the species level in this area. 2. Materials and methods 2.1. Description of study area Bah!ıa Todos Santos is located some 100 km south of the United States—Mexico border at

31 400 –31 560 N and 116 360 –116 500 W (Fig. 1). It has an area of approximately 116 km2. About 80% of the bay lies between 10 and 50 m depth. A narrow submarine canyon, reaching depths of 400 m, begins at the southwest entrance of the bay and extends between Punta Banda and Islas Todos Santos (Castro-Longoria and Hammann, 1989). The pattern of circulation within the bay generally consists of oceanic influxes of water from both the north and south, following the contour of the coast and forming a cyclonic gyre to the south and an anticyclonic gyre to the north (Alvarez-Sa! nchez et al., 1988; Argote-Espinoza et al., 1991). Mean surface temperature in the bay ranges from 11 C in February to 22.5 C in August and September. Surface salinity ranges from 33.7% in winter to 33.3% in summer (Mancilla and Mart!ınez, 1991). Bivalve aquaculture of the mussels Mytilus edulis and M. californianus takes place in the southern section of the bay. The creeks El Carmen, El Gallo, San Carlos, Ensenada and San Antonio have direct input into the bay, delivering fresh water run-off and sediments to the system (Avila, 1983; Rodr!ıguez-Villanueva et al., 2000). Sediment distribution in the bay, according to Emery et al. (1957) and Riveroll (1985), is characterized by three main facies: very fine sand to medium sand, mud to fine sand, and medium mud to clay. 2.2. Data collection Thirty-nine stations were sampled in October 1994 (Fig. 1) with a 0.1-m2 Van Veen grab from the oceanographic vessel Francisco de Ulloa. Physicochemical data of the water column were obtained using a CTD at each station. Environmental measurements included depth (m), temperature ( C), salinity (%) and dissolved oxygen (ml l1). For each station three grabs were sampled and sieved through nested 1.0- and 0.5-mm mesh screens. Organisms retained were fixed with a 7% buffered formalin solution. In the laboratory, each sample was washed through a 0.5-mm mesh screen and sorted under a stereoscopic microscope to different zoological groups. Organisms were preserved in 70% isopropyl alcohol. Polychaetes were

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Fig. 1. Study area in Baja California, with location of sampling stations.

identified to species level using different taxonomic keys (Blake, 1995; Blake and Hilbig, 1994; Blake et al., 1995, 1996; Fauchald, 1977; Gray, 1981; Hilbig, 1994; Knox, 1977; Salazar-Vallejo and Salaices-Polanco, 1989). Sediment organic content (%) and sediment particle size (+) were measured in the superficial sediment (2 to 3 cm) (Table 1). Organic matter content was determined by ignition loss (Dean, 1974; Byers et al., 1978). To determine sediment particle size sediments were homogenized and 50 g samples were dry-sieved through a series of mesh sizes (from 4.75 to 4 +) and mechanically shaken for 10 min. The sediments retained on each sieve were weighed and the percentage of each

! granulometric category was determined (RendonMarquez, 1995). Statistical methods were used to describe the structure and organization of the polychaete community within the bay. Diversity was calculated using Shannon’s Index (H 0 ) (Shannon and Weaver, 1963; Frontier, 1985); Pielou’s evenness index (J 0 ) (Pielou, 1977). Trophic groups were determined using Fauchald and Jumars (1979), Mangum et al. (1968) and Orth et al. (1984). Olmstead and Tukey’s test (Sokal and Rohlf, 1995) was applied to analyze spatial distribution of polychaetes species. This technique plots the frequency of appearance in each site sampled

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Table 1 Environmental parameters measured in Bah!ıa Todos Santos Station

Depth (m)

Temperature ( C)

Dissolved oxygen (ml L1)

Salinity (%)

Org. matter content (%)

Silt-clay (%)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 18 19 20 21 22 23 24 25 26 27 28 29 30 31 36 37 38 39 40 41 43 44 45 46 47

18.0 19.6 20.0 20.0 19.2 15.0 6.9 19.0 26.5 25.8 24.6 24.8 24.0 19.0 29.0 30.0 38.0 47.7 51.0 46.0 62.5 102.2 210.0 188.0 47.7 37.5 34.0 34.5 43.6 165.0 238.0 342.0 75.0 400.0 295.0 63.6 27.5 22.7 18.2

17.3 15.6 14.7 13.9 16.2 15.0 17.8 14.6 14.7 14.2 13.8 14.1 14.5 14.7 13.9 13.8 0.0 13.0 13.3 13.9 12.5 11.7 9.7 10.6 13.3 13.7 13.7 13.7 13.0 10.2 9.1 8.2 12.5 0.0 8.1 12.0 14.9 14.4 15.6

5.1 5.4 4.9 4.6 5.4 5.0 5.1 5.1 4.8 5.2 5.1 5.5 5.6 5.1 3.5 4.2 0.0 3.2 3.8 4.7 3.5 2.1 1.4 1.3 3.4 4.0 4.6 3.2 3.5 1.4 1.4 1.1 3.1 0.0 1.0 2.9 5.2 4.5 4.9

33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.4 33.5 33.5 0.0 33.5 33.5 33.4 33.6 33.8 34.2 34.0 33.5 33.5 33.4 33.5 33.5 34.1 34.2 34.2 33.6 0.0 34.2 33.7 33.4 33.4 33.4

2.0 1.5 0.9 0.5 1.2 0.9 1.3 1.8 1.2 1.6 1.0 1.3 3.1 1.9 1.3 0.9 2.8 3.2 2.3 2.2 4.4 2.3 9.1 6.1 2.0 1.8 0.0 0.0 1.5 7.4 5.6 10.6 4.8 0.0 0.0 3.6 1.1 2.1 2.3

92.9 96.9 98.1 1.2 95.7 95.4 73.3 94.5 86.5 96.8 98.3 98.1 20.4 78.2 99.0 98.9 83.0 96.0 95.1 87.3 78.8 40.3 60.6 84.6 97.4 97.9 0.0 0.0 32.9 88.0 95.5 84.4 14.8 95.8 98.4 98.4 98.4 91.1 91.1

expressed as percentage against the density of organisms for each species. A mean average was calculated for both axes, resulting in four quadrants: I—Frequent and abundant species, II— Non-frequent and abundant species, III—Nonfrequent and non-abundant species, and IV— Frequent and non-abundant species. Stress predictability (Alcolado, 1992) modeling was applied to establish the level of environmental

stress existing in the bay. Environmental severity or stress was predicted based on values of diversity (H 0 ) and equitability (J 0 ), coupled with different physico-chemical characteristics measured for each sample site. Alcolado adapted this technique from Preston and Preston (1975), who considered that the degree of stress is determined by the degree of temporal predictability in environmental conditions and the degree of physiological stress

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imposed by the physical environment. Either a temporally unpredictable or a temporally constant but physiologically stressful environment should constrain the development of high species diversity, since relatively few species would be able to colonize the environment successfully. However, the equitability in the distribution of individuals among species should be different in the two environments. In a constant but severe environment, equitability should be relatively high in late successional stages. As the species that have successfully adapted to the extreme environment begin to realize full exploitation of their available resources, they become progressively more ‘‘k selected’’ and this should lead to greater equitability. In contrast, in an unpredictable environment, catastrophic disturbances may keep the ecosystem at a low state of maturity; as a result, one would expect both species diversity and equitability to be low. Alcolado (1992) determined the thresholds based in a study of benthic organisms from 104 stations located in different biotopes. The association of certain values of diversity and equitability characterized different environments that correspond to different environmental conditions. Ordination and classification methods were used to detect spatial patterns among the polychaete fauna in the bay. The relationship between sample stations is reflected by the position they display in factorial space; when two stations were close to each other, they had more similar faunistic profiles (Frontier and Pichod-Viale, 1993; D!ıaz-Castan˜eda et al., 1993). A correspondence analysis was carried out on the faunistic data: 180 species and 39 stations. Some species with the lowest abundances were eliminated. Cluster analysis using Pearson and Bray–Curtis coefficients (Bray and Curtis, 1957; Sokal and Rohlf, 1995) was employed to evaluate the level of association of different stations and species. The raw data were transformed by using logðX þ 1Þ: In order to understand which environmental factors had the greatest influence on faunal composition and structure. Principal component analysis (PCA) was applied to a correlation matrix of six environmental variables: temperature, dissolved oxygen, depth, salinity, organic matter content,

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and percent silt, and then plotted in a twodimensional space. Non-metric multidimensional scaling (MDS) analysis applied to a matrix of 180 species abundances in 39 stations allowed for the detection of spatial patterns among the polychaete species that inhabit this bay. Species with low total abundance, 1 or 2 individuals were eliminated. PRIMER package described in Clarke and Warwick (1994) was used.

3. Results Analysis of the marine benthic samples demonstrated that 64% of all invertebrate macrofauna belonged to polychaetes, with 13,757 specimens representing 44 families and 203 species. Three families are reported as new records for Baja California: Aphroditidae (Aphrodita cf japonica), Pholoidae (Pholoe glabra, Pholoe sp.), and Fauveliopsidae (Fauveliopsis gabra). The best represented families in the bay were: Spionidae (23%), Capitellidae (12%), Paraonidae (8%), Cirratulidae (7%), Maldanidae (6%), Ampharetidae (5%), and Nephtyidae (5%). These families had the highest density values, which when combined, represented approximately 65% of the total polychaete fauna. Bah!ıa Todos Santos presented a high level of family richness, with at least 20 families present in 70% of sampled stations. The dominant species in Bahia Todos Santos belong mostly to the families Spionidae, Capitellidae, Paraonidae, Cirratulidae, Maldanidae, Orbiniidae, Nepthyidae, and Ampharetidae. Spionids were the most abundant polychaetes and included 16 taxa. Among the numerically dominant species were Mediomastus spp., Apoprionospio pygmaea, Nepthys cornuta, Lumbrinereidae UI, Leitoscoloplos pugettensis, Cirratulus cirratus, Aricidea (Aricidea) wassi, Praxillella pacifica, Spiophanes bombyx, S. duplex, Prionospio spp, Exogone lourei, Pectinaria californiensis, Pherusa neopapillata, Amphicteis scaphobranchiata, Glycera armigera, A. (Acmira) catherinae, A. (Acmira) simplex, A. (Allia) sp A, Levinsenia gracilis. Olmstead and Tukey’s graph is presented at family and species level. A selection of

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characteristic species was done in order to produce a clear graph (see Table 2). The 44 polychaete families and 203 species (Figs. 2a and b) were placed in three out of four possible categories: dominant, restricted and rare. In quadrant I (frequent and abundant), 18 polychaete families were characterized as dominant. Paraonidae, Spionidae, Nephtyidae, Onuphidae, and Goniadidae displayed high densities and wide distribution throughout the bay. The families Spionidae, Capitellidae, and Paraonidae presented the highest

densities, and when combined accounted for more than 50% of the total abundance of polychaetes. Seven families restricted to certain areas of the bay were located in quadrant II (non-frequent and abundant) and corresponded to 15% of all families. In quadrant III (non-frequent and nonabundant), 19 polychaete families were located, occurring at only one or two stations, such as Chrysopetalidae, Serpulidae, Amphinomidae, Sabellariidae, and Poecilochaetidae. No families were located in quadrant IV, corresponding to frequent

Table 2 Polychaete species abbreviations used in Fig. 3 Ne Pi Lp Lu Ms Ps Sb Mca El Ls Sd Ss As Pca Ga Lg Ap Aw Pp Ac Ph Mo Sm Gn Eh Mg Aa Lc Dt Am Su Gl Ly Ca Ew Mh Tr Eb

Nepthys caecoides Parapronospio pinnata Leitoscoloplos puggetensis Lumbrinereidae Mediomastus sp Prionospio sp Spiophanes bombyx Mediomastus californiensis Exogone lourei Laonice sp Spiophanes duplex Spiophanes sp Apoprionospio sp Pectinaria californiensis Glycinde armigera Levinsenia gracilis Apoprionospio pigmea Aricidea wassi Praxillela pacifica Acmira catherinae Pherusa neopapillata Melinna oculata Sabellides manriquei Glycera nana Ehlersia heterochaeta Myriochele gracilis Allia sp 1 Lanice conchilega Diopatra tridentata Amphicteis sp Spio maculata Glycera lapidum Lumrinerides platypygos Capitella complex Exogone dwisola Magelona hartmanae Terebellidae Exogone breviseta

Al Oe

On Si

St Lv

Py

My Allia sp A Et Onuphis elegans Par Pu Cf Ne Onuphidae Di Spiophanes berkeleyorum Ao Cs Gma Gm Gu Streblosoma sp B Lanassa venusta Pd Pc No Oi Ar Pr Polycirrus sp Nf Es Gl Au Pd Ae Pl Me Pm Pt Cg Ad Nc

Myriochele sp Eclysippe trilobata Paraonidae Pista sp C Cirrophorus furcatus Nepthys caecoides Diopatra sp Amaeana occidentalis Cossura sp A Glycera macrobranchia Glycera americana Glycera sp

Polydora sp Polydora cirrosa Nothria occidentalis Onuphis iridiscens Aricidea sp Piromis sp A Notocirrus californiensis Eusyllis sp Glycera lapidum Ampharete acutifrons Prionospio dubia Aglaophamus erectans Phylo sp Melinna heterodonta Pista moorei Pista brevibranchiata Clymenura gracilis Aglaophamus dicirrus Nephtys cornuta

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Fig. 2. Olmstead and Tukey’s analysis placed polychaetes families from Bah!ıa Todos Santos into three quadrants corresponding to dominant, restricted and rare.

and non-abundant families. Approximately 89% of species were located in quadrants I or III. Eight species were located in quadrant I L. puggetensis, Mediomastus sp., N. cornuta, Prionospio sp., S. bombyx, Paraprionospio pinnata, M. californiensis, and Lumbrineridae UI. 20 selected species appear in quadrant II, while 52 selected species are located in quadrant III (Fig. 2b). Bah!ıa Todos Santos exhibited a broad range of species richness per station. Values varied between 6 species (near the harbor) and 67 species (next to Estero Punta Banda). Higher species richness values (48 to 67 species per station) were located in the southern section of the bay (except station 13). Approximately, 30% of the stations presented a diversity H 0 value higher than 4.00, indicating this is an adequate environment for polychaetes (Woodin, 1974; Wilson, 1990). Diversity values ranged between 2.06 and 4.80, with higher values found also in the southern section of the bay, especially between Punta Banda and Islas Todos Santos, stations 24 and 40 (Fig. 3). In most of the stations, Pielou’s evenness index (Fig. 4) showed high values: 58% of the stations presented values higher than 0.80. However, some coastal stations (2, 4, 7, 9, 14) located close to the harbor and creeks seem relatively affected by freshwater

discharges and pollution; J 0 values ranged between 0.54 and 0.67. These stations were characterized by lower abundance and diversity values, and an increase in species belonging to Spionidae (Apoprionospio, Prionospio, Spiophanes), Capitellidae (Mediomastus), Orbiniidae (Leitoscoloplos), Cirratulidae (Cirratulus) and Maldanidae (Praxillella). Among the numerically dominant species, represented by more than 137 individuals (total abundance), in this study, were: Mediomastus spp., A. pygmaea, A. scaphobranchiata, P. pinnata, Sabellides manriquei, P. neopapillata, S. bombyx, Glycinde armigera, Lumbrineris spp., P. pacifica, N. cornuta, Chaetozone armata, Caulleriella sp., Cirriformia spirabrancha, Aphelochaeta monilaris, L. pugettensis, Myriochele sp., A. (Acmira) catherinae, A. (Acmira) simplex, A. (Allia) sp. A, A. (Aricidea) wassi, L. gracilis, P. californiensis, E. lourei, and Prionospio spp. Values of species diversity (H 0 ) and evenness (J 0 ) for stations sampled were analyzed and placed into four ‘‘environments’’ (Fig. 4) as defined by the stress-predictability modeling. Environment I, which included 26 stations with the highest values of diversity (H 0 ) (2.92–4.90) and evenness (J 0 ) (0.74–0.87), was characterized as being very favorable and stable. Environment II (stations

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Fig. 3. Species richness and diversity in Bah!ıa Todos Santos, Baja California.

38, 41), situated to the extreme southwest of the bay, was favorable and stable, H 0 values ranged between 2.92 and 3.90, and J 0 values between 0.73 and 0.86. Environment III (station 47, H 0 3.84, J 0 0.88) was characterized as being constant, with a degree of environmental stress. Finally, Environment IV, which included stations 2 and 39, was moderately favorable, with unstable conditions and a certain degree of environmental stress. Environment IV station diversity values (H 00 ) oscillated between 2.06 and 2.26, evenness values (J 00 ) from 0.55 to 0.62, and were the lowest of this study.

PCA showed that organic matter content, percentage of silt-clay, and depth accounted for 95.6% of the total variance for all environmental factors measured. This indicated that the bay could be divided into three different groups of stations (Fig. 5). Group PCA I corresponded to shallow and intermediate depth areas of the bay (stations 2, 3, 6–12, 14, 18–25, 29, and 44–47). Group PCA II included stations (13, 26, 27, 36–41, and 43) were situated mainly in the area of the submarine canyon. Finally, Group PCA III (stations 30, 31 and 4) corresponded to areas with the coarsest sediment grain size in the bay.

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Fig. 4. Stress-predictability modeling (Alcolado, 1992) in Bah!ıa Todos Santos. Stations are located in different environments: I Very favorable and stable, II favorable and stable, III constant with a degree of environmental stress, IV moderately favorable, unstable conditions and a certain degree of environmental stress.

Fig. 5. PCA spatial presentation of stations based on physico-chemical parameters.

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Stations 30 and 31 were located at the northwest area of the bay, station 4 was located next to the mouth of Estero Punta Banda. Analyzing the trophic composition, we found that 91 species were surface and subsurface deposit-feeders, 50 species carnivores, 36 species filter-feeders, and 24 species herbivores. By far the dominant trophic group corresponds to surface and subsurface deposit-feeders who exploit organic matter and its associated bacterio-algal popula-

tions. Considering that polychaetes play a key role in the energy flow within the trophic web, their abundance and species composition can influence the entire trophic structure of the bottom system in Bahia Todos Santos (Paiva, 1993; Petti et al., 1996). Dendrograms generated with Pearson and Bray–Curtis similarity coefficients formed species and stations groups. These groups separated stations in relation to their sediment particle size,

Fig. 6. Dendrogram resulting from classification analysis using Bray–Curtis coefficient (stations). R-mode.

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depth and location in the bay. The dendrogram resulting from classification analysis using Pearson coefficient (not shown here), separated five groups of stations: Group 1) 10 coastal stations, half in front of the harbor and the other half in front of Estero Punta Banda; Group 2) eight stations located next to stations of group 1, also along the coast-line; Group 3) 10 stations located mostly in the middle of the bay; and Group 4) seven stations situated in the submarine canyon area. Species common to this last group belonged mainly to the families Nephtyidae, Maldanidae, Paraonidae and Onuphidae. The two stations with the coarsest grain size (30 and 31) were associated together in Group 5, while stations 29 and 47 were isolated from all others. The Bray–Curtis analysis (Fig. 6) separated five groups of stations at the 62% level of similarity: B1 comprised only two stations located between Islas Todos Santos and Punta Banda, with low

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polychaete abundances (58–61 ind./station); B2 joined six stations located east of the submarine canyon, which also presented low abundances (63– 143 ind./station); B3 was formed by six stations located mostly in the northwest area. They presented the coarsest sediments and the lowest abundance values (20–140 ind./station), B4 was formed by ten stations in the southwest and northeast sections of the bay; this group had the highest abundance values (250–1434). Finally, B5 consisted of 15 stations, arranged in the shape of a triangle and presented intermediate abundance values (225–475 ind./station). MDS analysis applied to a matrix of 180 species and 39 stations presented stress values of 0.13, which indicated that the configuration was a good representation of the faunistic similarities between stations (Fig. 7). The analysis showed five distinct groups: Group MDS I included stations (1, 2–8, 12, 18, 19, 29, 45, 47), which corresponded to a

Fig. 7. Non-metric MDS spatial presentation of stations sampled in Bah!ıa Todos Santos, Baja California.

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Fig. 8. Correspondence analysis applied to polychaete abundances from Bah!ıa Todos Santos.

shallow band in north–south direction, next to the coastline, and a narrow tongue advancing to the west, these stations contained sediments with 90% silt-clay in average. Group MDS II was composed of stations 4, 9, 10, 11, 13, 14, 46, corresponding to a shallow middle portion of the bay and 68% of silt-clay content. Group MDS III isolated three stations situated in the northwest area of the bay (30, 31, 36) corresponding to the coarsest sediments, containing only 11% silt-clay. Group MDS IV included stations 20–25, 28, 40, 44, located in the southern section of the bay, with the shape of an inverted ‘‘C’’ (75% silt-clay). Finally, Group MDS V consisted of stations 26, 27, 37–39, 41, 43, located in the submarine canyon area and south of Islas Todos Santos, with sediments containing 86% silt-clay. The groups of stations separated by MDS are very similar to those generated with the Bray Curtis coefficient. A Correspondence analysis (Fig. 8) was applied to faunal abundances of 180 species  39 stations, the first two axes extracted nearly 47% of the total inertia: 32.3% and 15.4% respectively. In the factorial plane 1–2 point-species arranged along axis 1, with three extreme points: group A correspond to a group of species with an extensive distribution throughout the bay and relatively high abundances (Polydora ciliata, A. pygmaea, N. cornuta, Mediomastus spp., G. armigera, Typosyllis sp., Prionospio lighti), group B located in the negative side of axes 1 and 2 included species

present in the shallow areas of the bay, especially near the harbor and El Gallo Creek, with intermediate abundances (Spiophanes sp., S. bomby, Laonice cirrata, M. californiensis, Ampharete labrops, L. pugettensis, P. pinnata). Finally group C was formed by species at the extreme point of axis 1, present in the area of the submarine canyon (N. caecoides, Nothria occidentalis, Mooreonuphis sp. 1, Onuphis elegans, P. californiensis, A. (Acmira) simplex, L. gracilis, Notoproctus sp.). Axis 1 seems to separate species present in shallow and deep areas of the bay.

4. Discussion Polychaetes in Bah!ıa Todos Santos were characterized by a diverse composition, 44 families and 203 species; in other Pacific lagoons lower number of species have been reported: in Magdalena Bay in Baja California Sur, D!ıaz-Castan˜eda and de ! Leon-Gonz a! lez (submitted) report 25 families and 86 species; while in Barra de Navidad lagoon in Jalisco, Rodr!ıguez-Cagija (1993) collected 26 families and 35 polychaete species. In the bay of Antofagasta in Chile, Carrasco (1997) reported 90 polychaete species with Shannon diversity values fluctuating between 2.3 and 3.6. It is important to consider, when comparing studies, if they used the same sampling devices and mesh sizes to sieve the sediments. The values in Bah!ıa Todos Santos can

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be explained by an association of factors: a certain sediment heterogeneity, coupled with constant water circulation patterns and upwellings, which together promote species richness. Several authors emphasize the importance of availability of microhabitats in determining higher or lower levels of density and diversity (Platt and Shaw, 1983; VilloraMoreno, 1997). The presence of heterogeneous sediments and Macrocystis pyrifera in some areas of Todos Santos creates more potential niches. Approximately 30% of the stations presented H 0 values higher than 4.00, which can indicate that this is an adequate environment for polychaetes (Woodin, 1974; Wilson, 1990). The analysis of the trophic structure of benthic communities is important to determine energy flow in marine sediments. In the present study, surface and subsurface deposit-feeders were dominant; generally they were positively correlated with muddy sediments and organic matter content. They were more abundant in areas of low energy and consequently with high concentrations of organic matter as has been found by other authors (Bianchi and Morri, 1985; Tena et al., 1993). Polychaetes are frequently the main component of the benthic macrofauna, both in number of species and number of individuals. In addition, they play a key role in the macrobenthic secondary production on continental shelves (Paiva, 1993). In this study polychaetes were the dominant macrofauna group (64% of total macrofauna) and had the highest proportion of widespread species. Due to seasonality, however, the species identified as important (higher abundances) could be less important in other seasons than autumn, when the sampling was carried out. Depth-related patterns, which have been described by some authors (Skorowski et al., 1998; Bromberg et al., 2000; Ellingsen, 2002), were not observed in this study. In general, values of density and richness increased with depth except for the southwest section where the submarine canyon is located. Higher abundances were correlated with medium and fine-silty sediments, which also had higher concentrations of organic matter. The Allan Hancock Foundation surveys and other infauna studies in California (Barnard and Hartman, 1959; Jones, 1969; Oug, 1998) indicated

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that depth is the primary habitat factor organizing southern California benthic communities. Other infaunal studies (Snelgrove and Butman, 1994) have suggested that sediment type is a primary factor. Bergen et al. (2001), in a benthic survey on the southern California coast, analyzed data from 175 stations and found four habitat related infaunal assemblages: a shallow water assemblage from 10 to 32 m, a mid-depth assemblage between 32 and 115 m, and two deep-water (115–200 m) assemblages, one in fine and the other in coarse sediments. Benthic abundance and diversity were greatest in the mid-depth assemblage. Although depth and sediment grain size are usually important factors in the distribution of polychaetes, as Snelgrove and Butman (1994) and Bergen et al. (2001) suggested, the level of ambient energy and the amount of available organic matter are more likely to be primary driving forces, with depth and sediment grain size playing secondary roles. The energy profile of water flow immediately above the sediment–water interface determines the size of particles in surficial sediments, which in turns affects properties such as the ease of burrowing, which may limit the species that can survive. About 75% of the bay has high values of diversity, high values of evenness, and high species richness, all indicative of a favorable environment for polychaete development and a healthy benthic community (Snelgrove et al., 1997). Highest values of diversity were found at an intermediate depth; this observation is consistent with previous studies off the coast of California (Hyland et al., 1991; Thompson et al., 1993), although in the Atlantic coast, abundance and diversity increase as depth increases down to the continental rise at 2300– 2800 m (Neff et al., 1989). However, some coastal stations of Bahia Todos Santos, located close to the harbor and creeks seemed partially affected by freshwater discharges and pollution. These stations were characterized by lower abundance and diversity values, and an increase in species belonging to the families Spionidae, Capitellidae, Orbiniidae and Cirratulidae. The increase of these polychaetes (Capitella complex, Cirratulus, Dypolydora, Prionospio, Spiophanes etc.), particularly

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members from the first two families, is probably related to the increase in the organic matter content in sediments and may indicate stressed conditions. Grassle and Grassle (1976) and Tsutnumi (1987) reported that organically polluted areas represent natural habitats for some species of Capitellidae and Spionidae. An increase in the organic matter content of sediments can produce an increase of depositfeeding species, which are able to feed on detritus and its associated microorganisms. Some opportunistic species belonging to Spionidae, Capitellidae and Orbiniidae are able to exploit rapidly organic-rich sediments, increasing their densities in these disturbed areas. Seasonal upwelling fronts in this region (Gaxiola and Alvarez, 1986; Ibarra-Obando et al., 2001) increase the plankton biomass, part of which sinks and contribute to the accumulation of organics in sediments. This situation creates favorable conditions for the growth and reproduction of polychaetes and a high abundance of benthic organisms, especially deposit-feeders. Although different feeding guilds were represented, deposit-feeders were dominant. Sediment reworking activities characteristic of most depositfeeders play a significant role in oxygen diffusion. Tube builders also can play an important role in degradation of organic matter since most tube builders respire aerobically and actively pump the oxygen they need into the sediment. (Brown, 1975; Gallagher et al., 1983; Levin et al., 1997; Beesley et al., 2000). Muniz and Pires (1999) studied the trophic structure of the benthic community in the coast of Brazil, the ecosystem seems to be based on a detritus food web and there is a dominance of deposit-feeders polychaetes. The Olmstead and Tukey’s plot confirmed an irregular distribution of polychaetes within the bay. Distribution seems to be strongly related to sediment characteristics, as has been shown in other studies (Gray, 1974; Snelgrove and Butman, 1994). A heterogeneous sediment of varying particle sizes, can be expected to give more structural heterogeneity and potential niche space and therefore higher diversity as we found in Bah!ıa Todos Santos, particularly in the southern section of the bay. Principal component analysis of the

physico-chemical factors divided the bay in three different areas: shallow—medium depth, northwest area and submarine canyon area. This analysis established that granulometry, depth and organic matter content explain most of the variance. This support the results obtained with the similarity coefficients and the MDS analysis. The correspondence analysis applied to faunal abundances showed three groups of species (Fig. 8A–C) that seem to correspond to different polychaete assemblages located preferentially in the shallow habitat, mid-depth, and deep-water areas of the bay. This observation is consistent with other studies in the region (Fauchald and Jones, 1983; Thompson et al., 1993). MDS analysis corroborated results shown in dendrograms, confirming the separation between coastal-shallow stations, northwest stations characterized by the coarsest sediments, southernmiddle stations where the bivalve culture takes place and the submarine canyon (stations with more than 80% of silt-clay). Probably the biodeposition due to Mytilus cultures in long-lines located in the southern section of the bay contribute partially to the high values of diversity and abundances found in that area. In conclusion, Bahia Todos Santos hosts a rich annelid fauna of which polychaetes are the most important macrofauna group in terms of abundance and number of species, being extensively distributed in this bay. Species richness was variable, ranging from 6 to 67 species/station, the lowest values located near the harbor. Their distribution seems strongly related to location in relation to the coast-line, sediment characteristics, and percentage of organic matter. The bay is characterized by high diversity, and approximately 80% of stations were favorable environments for polychaetes, especially in the southern area where the bivalve culture takes place.

Acknowledgements ! for We thank R. Jime! nez and M. Mondragon their technical assistance in sorting samples and to all the people who took part in Bahia-I-10-94 cruise. Special thanks are given to C. Almeda for

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his help with software packages during data treatment, and two anonymous reviewers for his comments of the manuscript. Support for this

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! project was provided by Centro de Investigacion Cient!ıfica y Estudios Superiores de Ensenada (CICESE) and CONACYT.

Appendix Polychaete species found in Bah!ıa Todos Santos, Baja California. Family

Species

AMPHARETIDAE

Amage anops (Johnson 1901) Amage sp. UI Ampharete acutifrons (Grube 1860) Ampharete finmarchica (M. Sars 1864) Ampharete labrops Hartman 1961 Ampharetidae sp. SD 1 San Diego MBL 1999 Ampharetidae, UI Amphicteis scaphobranchiata Moore 1906 Amphicteis sp. Anobothrus bimaculatus Fauchald 1972 Asabellides lineata (Berkeley & Berkeley 1943) Eclysippe trilobata (Hartman 1969) Lysippe sp. A Williams 1985 Lysippe sp. B Williams 1985 Melinna heterodonta Moore 1923 Melinna oculata Hartman 1969 Mooresamytha bioculata (Moore 1906) Paramage scutata (Moore 1923) Sabellides manriquei Salazar-Vallejo 1996 Schistocomus hiltoni Chamberlin 1919 Schistocomus sp. A SCAMIT 1987 Sosane occidentalis (Hartman 1969)

APISTOBRANCHIDAE

Apistobranchus sp.

CAPITELLIDAE

Anotomastus gordiodes (Moore 1909) Capitella capitata complex Decamastus gracilis Hartman 1963 Heteromastus sp. Mediomastus sp. Mediomastus acuta Hartman 1969 Mediomastus ambisetus Hartman 1947 Mediomastus californiensis Hartman 1944 Notomastus latericeus M. Sars 1851 Notomastus sp. A SCAMIT 2001 Notomastus sp., UI

CALAMYZIDAE

Calamyzas amphictenicola Arwidsson 1932

CHAETOPTERIDAE

Phyllochaetopterus limicolus Hartman 1960 Spiochaetopterus sp. A Harris

COSSURIDAE

Cossura Cossura Cossura Cossura

modica Fauchald & Hancock 1981 rostrata Fauchald 1972 sp. A SCAMIT 1987 sp., UI

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Appendix (continued) Family

Species

FLABELLIGERIDAE

Flabelligeridae, UI Pherusa neopapillata Hartman 1961 Piromis sp. A Harris

GLYCERIDAE

Glycera Glycera Glycera Glycera Glycera Glycera Glycera Glycera

GONIADIDAE

Glycinde armigera Moore 1911 Goniada brunnea Treadwell 1906 Goniada littorea Hartman 1950 Goniada maculata Orsted 1843

HESIONIDAE

Gyptis sp. A Harris Heteropodarke heteromorpha Hartmann-Schroder 1962 Micropodarke sp. A Harris Podarkeopsis sp. A Velarde & Harris 1987 Podarkeopsis sp. D Velarde & Harris 1987

LUMBRINERIDAE

Lumbrinerides platypygos (Fauchald 1970) Lumbrineris californiensis Hartman 1944 Lumbrineris index Moore 1911 Lumbrineris limicola Hartman 1944 Ninoe tridentata Hilbig 1995 Scoletoma tetraura complex Lumbrineridae, UI

MAGELONIDAE

Magelona hartmanae Jones 1978 Magelona sacculata Hartman 1961 Magelona sp. B Harris

MALDANIDAE

Axiothella TS sp. 1 Harris Clymenella sp. A Harris Clymenella sp. Clymenura gracilis Hartman 1969 Euclymeninae sp. A SCAMIT 1987 Euclymeninae TS sp. 1 Harris Euclymeninae, UI juvenile Maldane sarsi Malmgren 1865 Metasychis disparidentata (Moore 1904) Notoproctus sp. A Harris Petaloclymene pacifica Green 1997 Petaloproctus sp. A Harris Petaloproctus sp. B Harris Praxillella pacifica E. Berkeley 1929 Rhodine bitorquata Moore 1923

NEPHTYIDAE

Aglaophamus dicirrus Hartman 1950 Aglaophamus erectans Hartman 1950

americana Leidy 1855 lapidum-complex macrobranchia Moore 1911 nana Johnson 1901 oxycephala Ehlers 1887 sp. B Harris sp. C Harris sp., UI

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Appendix (continued) Family

Species

Aglaophamus eugeniae Fauchald 1972 Aglaophamus sp. Nephtys caecoides Hartman 1938 Nephtys californiensis Hartman 1938 Nephtys cornuta Berkeley & Berkeley 1945 Nephtys ferruginea Hartman 1940 Nephtys sp. OENONIDAE

Arabella TS sp. 1 Harris Drilonereis sp. A SCAMIT 1998 Notocirrus californiensis Hartman 1944

ONUPHIDAE

Diopatra ornata Moore 1911 Diopatra splendidissima Kinberg 1865 Diopatra tridentata Hartman 1944 Diopatra sp. UI Hyalinoecia juvenalis Moore 1911 Mooreonuphis nebulosa (Moore 1911) Mooreonuphis veleronis (Fauchald 1980) Mooreonuphis TS sp. 1 Harris Mooreonuphis TS sp. 2 Harris Nothria occidentalis Fauchald 1968 Onuphis elegans (Johnson 1901) Onuphis iridescens (Johnson 1901) Onuphis TS sp. 1 Harris Onuphidae, UI Paradiopatra parva (Moore 1911) Paradiopatra TS sp. 1 Harris Rhamphobranchium longisetosum Berkeley & Berkeley 1938

ORBINIIDAE

Leitoscoloplos pugettensis (Pettibone 1957) Orbiniidae, UI Phylo felix Kinberg 1866 Phylo sp. Scoloplos acmeceps Chamberlin 1919 Scoloplos TS sp. 1 Harris

OWENIIDAE

Myriochele gracilis Hartman 1955 Myriochele sp. B Harris Myriochele sp. M SCAMIT 1985 Owenia collaris Hartman 1955

PARAONIDAE

Aricidea (Acmira) catherinae Laubier 1967 Aricidea (Acmira) horikoshii Imajima 1973 Aricidea (Acmira) lopezi Berkeley & Berkeley 1956 Aricidea (Acmira) simplex Day 1963 Aricidea (Allia) antennata Annenkova 1934 Allia sp. A SCAMIT 1996 Allia TS sp. 1 Harris Aricidea (Aricidea) wassi Pettibone 1965 Aricidea (Aricidea) sp. SD sp. 1 Barwick 1999 Cirrophorus branchiatus Ehlers 1908 Cirrophorus furcatus (Hartman 1957)

843

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Appendix (continued) Family

Species

Levinsenia gracilis (Tauber 1879) Paradoneis eliasoni Mackie 1991 Paraonidae, UI PECTINARIIDAE

Pectinaria californiensis Hartman 1941

PILARGIDAE

Ancistrosyllis cf. groenlandica McIntosh 1879 Sigambra sp. Sigambra. tentaculata (Treadwell 1941)

POECILOCHAETIDAE

Poecilochaetus sp.

SABELLIDAE

Jasmineira sp. B Harris Pseudofabricola californica Fitzhugh 1991

SABELLARIIDAE

Neosabellaria cementarium (Moore 1906) Sabellaria alcocki complex

SPIONIDAE

Apoprionospio pygmaea (Hartman 1961) Dipolydora cardalia E. Berkeley 1927 Dipolydora socialis (Schmarda 1861) Laonice cirrata (M. Sars 1851) Laonice nuchala Blake 1996 Malacoceros punctata (Hartman 1961) Microspio pigmentata (Reish 1959) Paraprionospio pinnata (Ehlers 1901) Polydora cirrosa Rioja 1943 Polydora sp. Prionospio (Prionospio) dubia Day 1961 Prionospio (Prionospio) jubata Blake 1996 Prionospio (Minuspio) lighti Maciolek 1985 Prionospio (Minuspio) multibranchiata E. Berkeley 1927 Prionospio sp Spio maculata (Hartman 1961) Spiophanes berkeleyorum Pettibone 1962 Spiophanes bombyx (Claparede 1870) Spiophanes duplex (Chamberlin 1919) Spiophanes fimbriata Moore 1923 Spiophanes sp.

STERNASPIDAE

Sternaspis fossor Stimpson 1854

SYLLIDAE

Autolytus sp. Ehlersia heterochaeta Moore 1909 Exogone breviseta Kudenov & Harris 1995 Exogone dwisula Kudenov & Harris 1995 Exogone lourei Berkeley & Berkeley 1938 Eusyllis habei Imajima 1966 Eusyllis sp. Eusyllis transecta Hartman 1966 Odontosyllis phosphorea Moore 1909 Pionosyllis articulata Kudenov & Harris 1995 Pionosyllis sp.

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Appendix (continued) Family

Species

Sphaerosyllis ranunculus Kudenov & Harris 1995 Syllides mikeli Kudenov & Harris 1995 Syllidae UI Typosyllis sp. TS 1 Harris Typosyllis sp. TS 2 Harris TEREBELLIDAE

Amaeana occidentalis (Hartman 1944) Eupolymnia heterobranchia (Johnson 1901) Lanassa venusta venusta (Malm 1874) Lanice cf. conchilega (Pallas 1776) Phisidia sp. A Harris Pista bansei Saphronova 1988 Pista brevibranchiata Moore 1923 Pista moorei Berkeley & Berkeley 1942 Pista sp. C Harris Polycirrus sp. A SCAMIT 1995 Polycirrus sp. TS 1 Harris Polycirrus sp., UI Streblosoma sp. B SCAMIT 1985 Terebellidae, UI

TRICHOBRANCHIDAE

Artacamella hancocki Hartman 1955 Terebellides californica Williams 1984 Terebellides sp., UI

References ! del ambiente Alcolado, M.P., 1992. Sobre la interpretacion marino mediante el empleo de los !ındices de diversidad y ! ogicas ! equitatividad. Cienias Biol 24, 124–127. Alvarez-S!anchez, L., Hern!andez, R., Durazo, R., 1988. Patrones de deriva de los trazadores lagrangeanos en la Bah!ıa de Todos Santos. Ciencias Marinas 14, 135–162. Argote-Espinoza, M.L., Amador, B., Morales, C., 1991. Distribuci!on de los par!ametros temperatura, salinidad y ! en la Bahia de Todos Santos, tendencias de la circulacion Baja California. In: CICESE (Ed.), Mem. CIBCASIO. Ensenada, Baja California, M!exico, pp. 3–30. Avila, S.G., 1983. Volumen de sedimentos aportados anualmente a la Bah!ıa de Todos Santos, Baja California por los arroyos El Gallo, San Carlos y Las Animas 1972–1973. Tesis Profesional, ESCM, UABC, Ensenada, Baja California, M!exico, 75pp. Barnard, J.L., Hartman, O., 1959. The sea bottom off Sta. Barbora California: biomass and community structure. Pacif. Nature 1, 1–16. Beesley, P., Ross, G., Galsby, C., 2000. Polychaetes and allies: the southern synthesis. Fauna of Australia, Vol. 4A,

Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. CSIRO Publishing, Melbourne, 465pp. Bergen, M., Weisberg, S., Smith, R., Cadien, D., Dalkey, A., Montagne, D., Stull, J., Velarde, R., Ranasinghe, J., 2001. Relationship between depth, sediment, latitude, and the structure of benthic infaunal assemblages on the mainland shelf of southern California. Marine Biology 138, 637–647. Bianchi, C., Morri, C., 1985. I policheti come descrittori della struttura trofica degli ecosistemi marini. Oebalia 11, 203–214. Blake, J., 1995. Family Sigalionidae. In: Blake, J.A., Hilbig, B., Scott, P. (Eds.), Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, Vol. 5. Santa Barbara Museum of Natural History, Santa Barbara, CA, pp. 189–206 Blake, J.A., Hilbig, B. (Eds.), 1994. Taxonomic atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, Vol. 4, The Annelida Part 1, Oligochaeta and Polychaeta: Phyllodocida (Phyllodocidae to Paralacydoniidae). Santa Barbara Museum of Natural History, Santa Barbara, CA, 377pp. Blake, J.A., Hilbig, B., Scott, P.H. (Eds.), 1995. Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and

ARTICLE IN PRESS 846

V. Dı´az-Castan˜eda, L.H. Harris / Deep-Sea Research II 51 (2004) 827–847

Western Santa Barbara Channel, Vol. 5, The Annelida Part 2, Polychaeta: Phyllodocida (Syllidae and Scale-Bearing Families), Amphinomida, and Eunicida. Santa Barbara Museum of Natural History, Santa Barbara, CA, 378pp. Blake, J.A., Hilbig, B., Scott, P. (Eds.), 1996. Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, Vol. 6, The Annelida Part 3, Polychaeta: Orbiniidae to Cossuridae. Santa Barbara Museum of Natural History, Santa Barbara, CA, 418pp. Bray, J.R., Curtis, T., 1957. An ordination of the upland forest communities in southern Wisconsin. Ecological Monographs 27, 325–349. Bromberg, S., Nonato, E., Corbisier, T., Varella-Petti, M., 2000. Polychaete distribution in the near-shore zone of Martel Inlet, Admiralty Bay. Bulletin of Marine Science 67, 175–188. Brown, S., 1975. Biomechanics of water-pumping by Chaetopterus variopedatus Renier: skeletomusculature and kinematics. Biological Bulletin, Marine Biological Laboratory Woods Hole 149, 136–150. Byers, S.C., Mills, E., Stewart, P., 1978. A comparison of methods to determine organic carbon in marine sediments with suggestions for a standard method. Hydrobiologia 58, 43–47. Castro-Longoria, E., Hammann, G., 1989. Biomasa y composici!on general de la comunidad de zooplankton en la Bah!ıa de Todos Santos, BC Mexico, durante el evento de El Nin˜o 1982–1983. Ciencias Marinas 15, 1–20. Carrasco, F., 1997. Sublittoral macrobenthic fauna off Punta Coloso, Antofagasta, northern Chile: high persistence of the polychaete assemblage. Bulletin of Marine Science 60, 443–459. Clarke, K., Warwick, R.M., 1994. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth Marine Laboratory, Plymouth. Dean, W., 1974. Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods. Journal of Sediment Petrology 44, 242–248. ! D!ıaz-Castan˜eda, V., de Leon-Gonz! alez, A., (submitted). Analysis of soft-bottom infaunal macrobenthic polychaetes from Bah!ıa Magdalena, Baja California Sur, Mexico. Estuarine, Coastal and Shelf Science, submitted for publication. D!ıaz-Castan˜eda, V., Frontier, S., Arenas, V., 1993. Experimental re-establishment of a soft-bottom community: utilization of multivariate analyses to characterize different benthic recruitments. Estuarine Coastal and Shelf Science 37, 387–402. Ellingsen, K.E., 2002. Soft-sediment benthic biodiversity on the continental shelf in relation to environmental variability. Marine Ecology Progress Series 232, 15–27. Emery, K., Grosline, D.S., Uchupi, E., Terry, R., 1957. Sediments of three bays of Baja California: Sebastian Viscaino, San Cristobal and Todos Santos. Journal of Sediment Petrology 27, 95–115. ! ˜ ez, E., 1990. Impacto de las Encalada-Fleitez, R., Mill!an-Nun aguas residuales industriales y dom!esticas sobre las comu-

! nidades bentonicas de la Bah!ıa de Todos Santos, BC. Ciencias Marinas 16, 121–139. Fauchald, K., 1977. The Polychaete Worms. Definitions and keys to the orders, families and genera. Science Series, Natural History Museum of Los Angeles County, Vol. 28. 188pp. Fauchald, K., Jones, G., 1983. Benthic macrofauna. In: Southern California baseline Studies and Analysis, Vol. III, Sciences Applications. La Jolla, CA, 442pp. Fauchald, K., Jumars, P., 1979. The diets of worms: a study of polychaete feeding guilds. Oceanography Marine Biology: An Annual Review 17, 193–284. Frontier, S., 1985. Diversity and structure in aquatic ecosystems. Oceanography and Marine Biology: An Annual Review 23, 253–312. Frontier, S., Pichod-Viale, D., 1993. Ecosystemes. In: Masson, S.A. (Ed.), Structure, Fonctionnement et Evolution. Paris, 447pp. Gallagher, E., Jumars, P., Trueblood, D., 1983. Facilitation of soft-bottom benthic succession by tube builders. Ecology 64, 1200–1216. Gaxiola, G., Alvarez, S., 1986. Productividad primaria del Pac!ıfico Mexicano. Ciencias Marinas 12, 26–33. Grassle, J., Grassle, J.P., 1976. Sibling species in the marine pollution indicator Capitella (Polychaeta). Science 192, 567–569. Gray, J.S., 1974. Animal-sediment relationships. In: Barnes, H. (Ed.), Oceanography and Marine Biology: An Annual Review, Vol. 12. London, Allen and Unwin, pp. 223–261. Gray, J., 1981. Animal-sediment relationships. Oceanography and Marine Biology: An Annual Review 12, 223–261. Gray, J., 1997. Marine biodiversity: patterns, threats and conservation needs. Biodiversity Conservation 6, 153–175. Hilbig, B., 1994. Family Nereididae. In: Blake, J.A., Hilbig, B. (Eds.), Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, Vol. 4. Santa Barbara Museum of Natural History, Santa Barbara, CA, pp. 301–327. Hyland, J., Batiste, E., Campbell, J., Kennedy, J., Kropp, R., Williams, S., 1991. Macroinfaunal communities of the Santa Barbara Basin on the California outer continental shelf and slope. Marine Ecology Progress Series 78, 147–161. Ibarra-Obando, S., Camacho-Ibar, V., Carriquiry, J., Smith, S., 2001. Upwelling and lagoonal ecosystems of the Dry Pacific Coast of Baja California. In: Seelinger, U., Kjerfve, B. (Eds.), Coastal Marine Ecosystems in Latin America, Ecological Studies, Vol. 144. Springer, Berlin, pp. 316–330. Jones, G., 1969. The benthic macrofauna of the mainland shelf of Southern California. Allan Hancock Monogr. Mar. Biol. 4, 1–219. Knox, G., 1977. The role of polychaetes in benthic soft-bottom communities. In: Reish, D., Fauchald, K. (Eds.), Essays of Polychaetous Annelids in Memory of Dr. Olga Hartman. Allan Hancock Foundation, Los Angeles, CA, pp. 547–604. Levin, L., Blair, B., de Masters, G., Plaia, W., Thomas, C., 1997. Rapid subduction of organic matter by maldanis polychaetes on the North Carolina slope. Journal of Marine Research 55, 595–611.

ARTICLE IN PRESS V. Dı´az-Castan˜eda, L.H. Harris / Deep-Sea Research II 51 (2004) 827–847 Liz!arraga-Partida, L., 1974. Organic pollution in Ensenada Bay, Mexico. Marine Pollution Bulletin 5, 109–112. Mancilla, P.M., Mart!ınez, G.M., 1991. Variaci!on estacional de temperatura, salinidad y ox!ıgeno disuelto en la Bah!ıa de ! Todos Santos, BC, M!exico. Revista de Investigacion Cient!ıfica 2, 33–45. Mangum, C., Santos, S., Rhodes, W.R., 1968. Distribution and feeding in the onuphid polychaete Diopatra cuprea (Bosc). Marine Biology 2, 33–40. Muniz, P., Pires, A.M., 1999. Trophic structure of polychaetes in the Sao Sabastino Channel (SE Brazil). Mar. Biol. Berlin 134, 517–528. ! Mun˜oz Palacios, L., 1993. El sistema bentonico sublitoral en las costas del Pac!ıfico Norte: Campan˜as TOES (Febrero 1987). Tesis Maestr!ıa, CICESE, Ensenada, Baja California, M!exico, 636pp. Neff, J., Bothner, M., Maciolek, N., Grassle, J.F., 1989. Impacts of exploratory drilling for oil and gas on the benthic environment of Georges Bank. Marine Environment Research 27, 14–77. Orth, R., Heck, K., van Montfrans, J., 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator–prey relationships. Estuaries 7, 339–350. Oug, E., 1998. Relating species patterns and environmental variables by canonical ordination: an analysis of softbottom microfauna in the region of Tromso, Norway. Marine Environmental Res. 45, 29–45. Paiva, P.C., 1993. Trophic structure of a shelf polychaete taxocoenosis in southern Brazil. Cahiers de Biologie Marine 35, 39–55. ! P!erez Pen˜a, M., 1994. El sistema bentonico sublitoral en la costa norte del Pac!ıfico M!exico- E.U.A.: Campan˜a ECOBAC III 0690. Tesis Maestr!ıa, CICESE, Ensenada, Baja California, M!exico, 89pp. Petti, M.A., Nonato, E.F., Paiva, P.C., 1996. Trophic relationships between polychaetes and brachyuran crabs on the southeastern Brazilian coast. Revista brasilen˜a de Oceanograf!ıa 44, 61–67. Pielou, E.C., 1977. Mathematical Ecology. Wiley, New York, 385pp. Platt, H., Shaw, K., 1983. The detection of differences among assemblages in marine benthic species based on an assessment of dominance and diversity. Journal of Natural History 17, 859–874. Preston, E., Preston, J.L., 1975. Ecological structure in a West Indian gorgonian fauna. Bulletin of Marine Science 25, 248–258. ! Rendon-Marquez, G., 1995. T!ecnicas petrogr!aficas para el estudio de rocas y sedimentos en el Laboratorio de Petrolog!ıa del CICESE. Informe T!ecnico Acad!emico Serie Geolog!ıa, CICESE, 33pp. Riveroll, S.E., 1985. Distribuci!on de la materia org!anica en la Bah!ıa de Todos Santos, Baja California. Tesis Profesional ESCM, UABC, Ensenada, Baja California, M!exico, 87pp.

847

Rodr!ıguez-Cagija, S., 1993. Macrofauna de la laguna Barra de Navidad, Jalisco, pp. In: Salazar-vallejo, S., Gonzalez, N.E. (Eds.), Biodiversidad Marina y Costera de Mexico. Comision Nacional para la Biodiversidad y CIQRO, Mexico, pp. 499–508. Rodr!ıguez-Villanueva, V., D!ıaz-Castan˜eda, V., Mart!ınez, R., 2000. Structure and composition of the benthic polychaete families in Bahia Todos Santos, Baja California, Mexico. Bulletin of Marine Science 67, 113–126. Salazar-Vallejo, S., Salaices-Polanco, H., 1989. Poliquetos ! (Annelida: Polychaeta) de M!exico. University of Auton, Baja California Sur, La Paz, BCS M!exico, 229pp. San˜udo-Wilhelmy, S., Rivera-Hinojosa, I., del Valle, J., 1985. ! marina en la Bah!ıa de Estado actual de la contaminacion Todos Santos, BC Di!agnostico y alternativas para su ! y control. Reporte T!ecnico 85-01, UABC, reduccion ! Instituto Investigaciones Oceanologicas, pp. 7–32. Shannon, C.E., Weaver, W., 1963. The Mathematical Theory of Communication. University of Illinois Press, Urbana, 125pp. Skorowski, R., Corbisier, T., Robles, F., 1998. Meiofauna along a coastal transect in Admiralty Bay, King George Island. Pesquer!ıa Ant!artica Brasilen˜a 3, 117–132. Snelgrove, P., 1998. The biodiversity of macrofaunal organisms in marine sediments. Biodiversity and Conservation 7, 1123–1132. Snelgrove, P., Butman, C.A., 1994. Animal–sediment relationships revisited: cause versus effect. Oceanography and Marine Biology: An Annual Review 32, 111–177. Snelgrove, P., Blackburn, T., Hutchings, P., Alongi, D., 1997. The importance of marine sediment biodiversity in ecosystem processes. Ambio 26, 578–583. Sokal, R., Rohlf, F.J., 1995. Biometry. Freeman, New York, 887pp. Tena, J., Capaccioni, R., Torres-Gavila, F., Porras, R., 1993. An!elidos Poliquetos del antepuerto de Valencia: distribuci! y categor!ıas troficas. ! on Publicaciones especiales Instituto Espan˜ol de Oceanograf!ıa 11, 15–20. Thompson, B., Dixon, J., Schroeter, S., Reish, D., 1993. Benthic invertebrates. In: Dailey, M., Reish, D., Anderson, J. (Eds.), Ecology of the Southern California Bight: A Synthesis and Interpretation. University of California Press, Berkeley, pp. 369–458. Tsutnumi, H., 1987. Population dynamics of Capitella capitata (Polychaeta: Capitellidae) in an organically polluted cove. Marine Ecology Progress Series 36, 139–149. Villora-Moreno, S., 1997. Environmental heterogeneity and the biodiversity of interstitial Polychaeta. Bulletin of Marine Science 60, 494–502. Wilson, W., 1990. Competition and predation in marine softsediment communities. Annual Review of Ecology and Systematics 21, 221–241. Woodin, S., 1974. Polychaete abundance patterns in a marine soft-sediment environment: the importance of biological interactions. Ecological Monographs 44, 171–187.