Please note that this is the English translation (with original title) to:
2008. Opistobranquios. In: Danemann, Gustavo D., y Exequiel Ezcurra (eds.), Bahía de los Ángeles: Recursos Naturales y Comunidad. Línea Base 2007. SEMARNAT, Pronatura Noroeste, SDNHM & Instituto Nacional de Ecología, México. Pp. 319-338.
Figures and tables in original publication are accessible at: http://www.ine.gob.mx/publicaciones/consultaPublicacion.html?id_pub=546
Ten-Year Baseline Study of Annual Variation
in the Opisthobranch (Mollusca: Gastropoda) Populations at
Bahía de los Ángeles, Baja California, México
Research Associate, California Academy of Sciences, 192 Imperial Beach Blvd., # A, Imperial Beach, CA 91932, USA,
With gratitude, affection and respect, I dedicate this work to Rosa del Carmen Campay–Villalobos, Tom Smith, and the people of Bahía de los Ángeles.
IN MEMORIAM: Benjamin Casillas López (1976–2007)
“The shores of the Gulf, so rich for the collector, must still be fairly untouched....We had not the time for the long careful collecting which is necessary before the true picture of the background of life can be established.” (John Steinbeck, 1941, The Log from the Sea of Cortez)
From January 1992–December 2001 research dives were conducted at two shoreline sites north of the town of Bahía de los Ángeles (BLA), Baja California, using the total density per unit of time. This yielded 6095 specimens of opisthobranch molluscs, and approximately 81 species.
Nine species were each encountered over 100 times, totaling 4999 specimens (82 % of the total number). Regression analyses on these species showed that over all the density of species per year significantly increased (P< = 0.01), but the number of specimens significantly decreased (P <= 0.007).
Comparisons of 8 species of Chromodorididae nudibranchs between sites at BLA and Punta Arenas/Isla Cerralvo, Baja California Sur, indicate higher densities and larger total body lengths for 2 species.
Baseline studies of the marine invertebrate fauna of Bahía de los Ángeles (BLA) are especially important to provide information that can be used to support the establishment of a natural park in this region, to establish guidelines for biodiversity conservation, and to monitor changes after the establishment of this reserve. In fact, as Hendriks et al. (2006) write, “We must improve our understanding of how the global ocean ecosystem works in order to design networks of protected areas that effectively preserve biodiversity.”
Habitat descriptions throughout the Sea of Cortez
Descriptions of the general biology, physiography and physical environment, and the lower intertidal and subtidal rocky reef zones at BLA and throughout the Sea of Cortez can be found in references such as Roden & Groves (1959), Barnard & Grady (1968), Robinson (1973), Brusca (1980), Bertsch (1991) and others. Schwartzlose et al. (1992) provide a comprehensive bibliography for the Sea of Cortez.
Molluscan studies at Bahía de los Ángeles
For many years, our knowledge of the molluscan fauna of BLA has been based primarily on sporadic collections or taxonomic lists of species collected over a wide range of localities throughout the bay, but without continuous monitoring of specific locations (e.g., see Steinbeck & Ricketts, 1941; McLean, 1961; Coan, 1968; Poorman & Poorman,1978; and Hertz, 1978 a, b). The resource sustainability of Modiolus capax (Conrad, 1837) is briefly discussed by Farmer (1990), and García–Aguirre & Buckle–Ramirez (1989).
Two references to the fishery of the scallop Pecten vogdesi Arnold, 1906, give quite contradictory statements. Coan (1973) states “the fishery [is] apparently quite successful,” whereas Wolfson (1970) writes “a study of the disappearance of edible clams from this area is carried out by the author.” It is important to emphasize that this fishery has not existed in the BLA region for over 25 years (pers. obser.) because of over harvesting of the resource.
Other molluscan bivalve studies include Serrano–Guzman & Avalos–Borja, 1991 (clam larval stages), and Islas–Olivares, 1982 (regarding the cultivation of the Japanese oyster, Crassostrea gigas).
Short-term taxonomic studies have provided most of our knowledge about the opisthobranch fauna. The type localities of 11 named species are in this region: Okenia angelensis Lance, 1966 (named from the “lowest intertidal zone, Bahía de los Ángeles”); Cerberilla pugnoarena Collier & Farmer, 1964, and Eubranchus cucullus Behrens, 1985 (both named from Puerto Refugio, Isla Ángel de la Guarda); Nembrotha hubbsi Lance, 1968 (Isla la Ventana), now a junior synonym = Tambja eliora (Marcus & Marcus, 1967); Cuthona longi Behrens, 1985 (Isla Raza); and 5 species from Punta la Gringa: Bajaeolis bertschi Behrens & Gosliner, 1988; Polycerella glandulosa Behrens & Gosliner, 1988; Trapania goslineri Millen & Bertsch, 2000; Peltodoris lancei Millen, in Millen & Bertsch, 2000; Okenia angelica Gosliner & Bertsch, 2004; and Dendrodoris stohleri Millen & Bertsch, 2005.
Long-term subtidal opisthobranch studies in this region have been reported by Bertsch, 1995, 2002 (natural history of Doriopsilla gemela); Bertsch, et al., 1998 (differences in community structures between Punta La Gringa/Cuevitas and Island/Puerto Don Juan sites); and Gosliner & Bertsch, 2004 (annual and monthly density variations, 1992–2001, of Okenia angelica).
This present work is a 10-year baseline study of the opisthobranch populations at two shore sites approximately 10 km north of the town of BLA, to enable future comparisons to be made regarding the health of or changes in these populations. This is the first long-term data set of the annual occurrences and variations among species and specimens for a group of marine invertebrates at BLA.
Importance and Selected Examples of Longitudinal Studies
Long-term longitudinal studies are increasingly becoming recognized as significant in determining population extinctions, habitat degradation, and resource management. Among various long-term studies in other regions and habitats. Thomas et al. (2004) and Foster & Aber (2004) describe repetitive community surveys of terrestrial plants, birds and butterflies. Diller (2004) and Milius (2004) discuss population variations in the mollusc-eating penguin Spheniscus magellanicus (Forster, 1781) and killer whales (Orca).
For decades, amateur aficionados have been providing significant density and diversity data for birds (Audubon Bird Count: www.audubon.org/bird/cbcl ) and marine fish (Great Annual Fish Count: www.fishcount.org ).
Historical overfishing and the recent collapse of coastal ecosystems are described in Jackson et al. (2001) and Lotze et al. (2006). Numerous government and academic investigators are conducting long-term studies on members of coral reef communities. Topics have included coral recovery after major predation events (Walbran et al., 1989), the decline of coral reef ecosystems (Pandolfi et al., 2003), the effects of coral decline on fish biodiversity (Jones et al., 2004), and the future of coral reefs due to marine protected areas (Mora et al., 2006) and major limitations of reproductive failure, habitat degradation and fragmentation, and the role of sea temperature changes in coral bleaching (Knowlton, 2001).
Published studies on opisthobranchs mainly involve temperate water intertidal locations. Todd (1981) and Trowbridge (2002) provide summaries and bibliographic sources. Trowbridge (1993) studied the population structure of two species of sacoglossan during a 4-month span. Nybakken (1974 and 1978) studied the abundance, diversity and temporal variability in central Californian intertidal nudibranchs over 27-month and 40-month periods.
Materials and Methods
In this survey within the synecdochic BLA, two sites accessible from the shore were studied: Punta la Gringa (29E 02.57' N’; 113E 32.3' W) and Cuevitas (29E 03.39' N; 113E 32.37' W). These sites are less than one nautical mile apart and are approximately 10 km north of the small fishing and tourist town of BLA. Both study sites have rocky basalt reefs and sandy/mud/silt and fine-grained rock and shell substrates (Bertsch, 1991).
In the 10 year period from January 1992–December 2001, the author made 211 research dives, totalling 229.3 hours of search time. During each research dive, every opisthobranch specimen was identified, counted and measured. Camacho–García et al. (2005) and Behrens & Hermosillo (2005) provide descriptions and color photographs of all species. Data collected by safety diving partners were not used in this analysis to ensure rigorous and similar control over quality of data collection. Actual collection of specimens was the barest minimal for taxonomic purposes, so as not to skew the data by withdrawal of the populations’ members.
The method of density study used related the number of specimens and species per unit of time searched (Nybakken, 1974, 1978). This method is statistically and realistically better in observing/finding opisthobranchs (rather than the traditional transect and quadrant system) because of the highly random distributional patterns of these organisms.
During the 10-year period from January 1992–December 2001, 6095 specimens of opisthobranch molluscs were counted and identified at these 2 sites, with a total count of at least 81 species (some were not identifiable, and some may actually include more than 1 species, because of difficulty in identification).
Table 1 lists total numbers of specimens for each species, total specimens and search time, and total specimen and species density throughout the entire 10-year period.
Bahía de los Ángeles endures a significant change in near surface sea water, from 58E to 83E F (14E–28E C) throughout the year (Robinson, 1973). This extreme water temperature variation, plus nutrient upwelling effects, contribute to the high numbers of species at these two study sites.
There is a distinct blend of species from two different faunal provinces: the tropical eastern Pacific, and temperate California. Species from this latter region occur north of the provincial boundary located in the area of Bahía Tortugas, Punta Eugenia, Isla Cedros and Bahía Sebastián Vizcaino, whereas Panamic species typically occur south of Bahía Magdalena (Keen, 1971). The region in between can be considered a provincial ecotonal boundary (Bertsch, 1993) where both groups of species might be expected to occur. Out of 75 clearly identified species, 44 (58.6 %) are only Panamic, and 31 (41.3 %) are well-known Californian species recorded north of the provincial ecotonal region. Note that several of these former species may occur north of this ecotone only during periods of El Niño. There are also Indo-Pacific species such as Berghia major, Eubranchus misakiensis, and Phestilla lugubris (see Skoglund, 2002, for additional references), and circumtropical species such as Limenandra nodosa (Bertsch, 1972, 1979).
Collier & Farmer (1964) reported a Caribbean species, Dendrodoris atropos (Bergh, 1879), in the Sea of Cortez, but the name is a junior synonym (see Keen, 1971) of D. krebsii (Mörch, 1863). These eastern Pacific specimens are now considered a synonym of D. fumata Rüppell & Leuckart, 1830, an Indo-Pacific species (Behrens, 2004).
Table 2 summarizes the data from the 22 most commonly found species (>25 specimens): hours searched, the total numbers of species and density, and total numbers of specimens and density per year. For each of them, Tables 4–13 (Online Supplemental Material: www.slugsite.us/hans/Hans_Page_01.htm ) present the number of specimens and density per hour during each of the 10-year search periods. These data are provided to allow future researchers the ability of comparing or contrasting data with future long-term studies.
Statistical analyses were made on the 9 species (Aeolidiella chromosoma, Berthellina ilisima, Dendrodoris fumata, Doriopsilla albopunctata, Doriopsilla gemela, Elysia diomedea, Histiomena convolvula, Phestilla lugubris and Phidiana lascrucensis) observed more than 100 times during the 10-year study period (the numbers upon which these analyses are based are found in the Online Supplemental Material). These 9 species were analyzed because of their numerical dominance in the community. The 4999 specimens of these 9 species represent 82 % of the opisthobranch fauna at these locations.
Regression analyses of the search data present significantly different results between the density of species and specimens during this time period. Figure 1 graphs the correlation between the density per hour of numbers of species per year. The coefficient is 0.071, and there is a clear level of significance (P <= 0.01). The correlation between the density per hour of numbers of specimens per year is opposite, having a negative slope (fig. 2a), with a coefficient of –0.07, at a high level of significance (P <= 0.007).
Hence, during a 10-year span (1992–2001), the total density of these 9 species increased, but the total density of specimens decreased. Differences for both results for all organisms observed (using the density per hour searched method) were statistically significant.
Among each individual species, there were two different density patterns: 7 species (accounting for 2845 specimens) exhibited no statistically significant change in density during this period. As representative of these species, the regression slope for Aeolidiella chromosoma is illustrated in figure 2b (r = 0.0018, P >= 0.958). The regression data for the other six species (which show a lack of significant correlation, i.e., no change in density) are: Berthellina ilisima (r = –0.04, P > = 0.395); Dendrodoris fumata (r = –0.046, P >= 0.12769); Doriopsilla gemela (r = –0.12769, P >= 0.0839); Doriopsilla albopunctata (r = –0.08379, P >= 0.144); Histiomena convolvula (r = –0.052, P >= 0.08); and Phidiana lascrucensis (r = 0.007, P >= 0.86). These 7 species did not contribute significantly to the decline in density of the largest cohort of opisthobranchs from 1992–2001. Their densities basically remained the same throughout the period.
Two species (accounting for 2154 observed organisms) exhibited significant declines in their population density. The Porites coral-eating Phestilla lugubris (fig. 2c) had a regression coefficient of –0.1044 (P <= 0.0476).
Most important was the major, dramatic decline in the population density of Elysia diomedea (fig. 2d). The regression coefficient is –0.16991 (P < = 0.0004).
The significant decline in density is due to the effect of combining together all data from the first set of 7 species with the large numbers of observed specimens of Elysia diomedea and Phestilla lugubris which presented very large and precipitous drops in density of specimens. From 1992–2001 the densities/hour for E. diomedea and P. lugubris declined respectively from 64.96 to 0.41, and from 3.85 to 0.47.
The taxonomy and natural history of these 2 opisthobranch species are distinctly different.
The sacoglossan Elysia diomedea feeds on marine algae, cell by cell, sucking out the contents and then passing the fully functional chloroplasts throughout their body, where these organelles photosynthesize and supply nutrients nutrients to the slug. Whether variations in thermo-hydrographic conditions, algal densities or habitat quality contributed to this decline, or whether this is just a normal population cycle is yet unknown.
The aeolid nudibranch Phestilla lugubris feeds on corals (in the Sea of Cortez, Porites californica Verrill, 1868, laying its eggs very close to the prey (usually under rocks). Until more closely-monitored future surveys are undertaken, this decline cannot be explained. As previously discussed (cf. selected examples of longitudinal studies), patterns of decline have occurred worldwide in tropical subtidal ecosystems.
Addenda: Density and Size Comparisons of Chromodorididae throughout the Sea of Cortez and at Bahía de los Ángeles
Genera and species of Chromodorididae are almost always tropical in distribution. Even though the opisthobranch fauna of BLA is primarily (58.6 %) tropical eastern Pacific (= Panamic faunal province), only 66 of the 6095 total specimens were identified as members of the chromodorid genera Chromodoris, Glossodoris, Hypselodoris and Mexichromis (0.0108 %). Of the 8 species at the BLA study sites (table 1), Chromodoris norrisi was recorded 32 times (total density of 0.13955 specimens per hour), whereas Hypselodoris ghiselini only 16 times (total density of 0.0698 per hour).
In another study (pers. obser., April and June 1985), the densities per hour of Chromodoris norrisi and Hypselodoris ghiselini were reversed, being respectively 5.97 and 16.1 times greater in the extreme southern part of the Sea of Cortez (Las Arenas, 24E 03' N; 109E 49' W, and Isla Cerralvo, ~ 24E 08' N; 109E 49' W ). As part of that comparative study, these species were longer at these Baja California Sur locations than at BLA. At BLA and Las Arenas/Isla Cerralvo respectively, the average total body sizes of C. norrisi were 12.77 mm and 19.18 mm; and those of H. ghiselini were 31.66 mm and 46.32 mm.
During a curtailed study period at BLA, from January 1992–December 1997 (table 3), Chromodoris norrisi was more frequent and had a greater total body length during the early summer months of June and July, despite the fact that the sea surface temperature is warmest (most tropical) in August and September (Robinson, 1973).
Dr. Jeff Crooks, Research Coordinator at the Tijuana River National Estuarine Research Reserve, provided me with the statistical analyses and graphs.
In addition to all who participated as safety diving partners over the years at Punta la Gringa and Cuevitas, I am especially grateful to those who often accompanied me underwater during this 10-year study period: Tom Smith, Michael D. Miller, Brian Coleman and Alan Grant; friends and colleagues above and below the water’s surface! I thank my dear friends at BLA: José Estrada, Delia Oleta, Carolina Espinoza, and Antonio and Bety Resendiz. To them, and many others who drove the Peninsular Highway with me, ¡un abrazo afectuoso y fuerte!
I thank my wife, Rosa del Carmen Campay, para su entendimiento y apoyo.
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Online Supplemental Material (Tables 4–13)