Revista Chilena de Historia Natural 73:797-830, 2000

Diversity, dynamics and biogeography of Chilean benthic nearshore ecosystems: an overview and guidelines for conservation

Diversidad, dinámica y biogeograffa del ecosistema costero bent6nico de Chile: revision y bases para conservaci6n marina

1 2 3 2 MIRIAM FERNANDEZ • , EDUARDO JARAMILL0 , PABLO A. MARQUET , CARLOS A. MORENO', SERGIO A. 1 2 2 6 NAVARRETE • , F. PATRICIO OJEDA , CLAUDIO R. VALDOVINOS' & JULIO A. VASQUEZ (*)

1 Estaci6n Costera de Investigaciones Marinas, Facultad de Ciencias Biol6gicas, Pontificia Universidad Cat6lica de Chile, Casilla 114-D, Santiago, Chile, e-mail: [email protected] 2 Departamento de Ecologfa, Facultad de Biologfa, Pontificia Universidad Cat6lica de Chile, Casilla 114-D, Santiago, Chile, 3 Instituto de Zoologfa, Universidad Austral de Chile, Valdivia, Chile, 4 Instituto de Ecologfa y Evoluci6n, Universidad Austral de Chile, Valdivia, Chile, 5 EULA, Universidad de Concepci6n, Concepci6n, Chile, 6 Universidad Cat6lica del Norte, Coquimbo, Chile, * in alphabethical order from the second to the last author

ABSTRACT

Despite Chile has been one of the pioneering countries in studies of human impact on marine communities, and despite the enormous economic and social significance that the marine environment has for the country, the development of marine conservation programs and the scientific basis for sustainability has not kept pace, with the exploitation rate of marine fisheries and the increasing use of the coast for other purposes. Although we think that the establishment of any conservation policies along the vast coastline of Chile must be based on a multitude of approaches and considerations, scientific, biological, and ecological principles should guide much ofthese efforts. In this paper, we attempt to present a general overview of the current knowledge about the ecology and biogeography of nearshore systems in Chile. Based on the most relevant existing information, our goals are to: 1) Identify major biogeographic and ecological features of nearshore ecosystems, and the obvious gaps in information, 2) identify the most harmful human activities impacting the structure and dynamics of these systems, and 3) suggest the possible use of indicators to assess the conservational status of different environments along the coast. This overview shows, on one side, the geographic areas of deficitary knowledge on nearshore environments that are critical for future marine conservation and management plans, and on the other, the availability of high quality information for other geographic areas along the coast. Regarding the taxonomy and large-scale patterns of species distribution, important gaps in information were detected, however no big changes in the total number of species are expected in the future. There are few large-scale patterns of species distribution are reported in the literature, and in this contribution, but more work needs to be done, particularly for some taxa, to identify areas of high species diversity as well as areas which possess unique characteristics in terms of ecosystem processes (e.g., particular disturbance and upwelling regimes in coastal marine ecosystems) and species (e.g., endemic and keystone species). For most marine invertebrates and macroalgae, hotspots in species diversity are present in southern Chile. New studies addressing the causal factors generating these large-scale patterns of species distribution are also needed; information about coastal oceanography and larval supply is still poor. This information crucial for the design of a marine reserve network. The information available on community structure and ecosystem functioning, especially highlighting the effect of human impact, comes from very few geographic regions. More information about community structure for other areas of the coast is required, particularly considering the strong differences in temperature, circulation patterns, habitat heterogeneity, species composition, as well as of upwelling and El Nifio effects along the 4,000 km of coastline. Finally, we list what we think are the most harmful human activities by area and environment along the coast, and integrate this information to suggest possible environmental indicators, and basic needs and guidelines for marine conservation in Chile.

Key words: Chile, marine conservation, biogeographical patterns, community structure, human impact.

RESUMEN

A pesar de que Chile ha sido un pafs pionero en estudios del efecto del impacto humano sobre la estructura comunitaria en ambientes marinos, y a pesar de la enorme importancia econ6mica y social que el ambiente marino tiene para el pafs, el desarrollo de programas de conservaci6n marina y de bases cientfficas para la sustentabilidad no se han generado a la misma tasa a la que han explotado Ios recursos y se ha utilizado el ambiente costero para diversos fines. Aunque nosotros pensamos que el establecimiento de planes de conservaci6n a lo largo de la costa de Chile debe basarse en varios factores, Ios principios cientfficos, biol6gicos y ecol6gicos deben guiar muchos de estos esfuerzos, y en este trabajo nosotros intentamos presentar una vision general del estado actual del conocimiento sobre la ecologfa y la biogegraffa del sistema costero en Chile. En base a la informaci6n más relevante existente, nuestros objetivos son: 1) 798 FERNANDEZ ET AL. identificar !as caracteristicas biogeognificas y ecol6gicas del ecosistema costero y tambien vacfos en informaci6n, 2) identificar !as actividades humanas más dafiinas que tengan impacto en la estructura y dinamica de estos sistemas, y 3) sugerir el uso de posibles indicadores para determinar la situaci6n de diferentes áreas de la costa de Chile, y !as necesidades de conservaci6n. Esta revision muestra, por un !ado, áreas geográficas con informaci6n crftica deficitaria para planes futuros de manejo y conservaci6n marina, y por el otro !ado, la disponibilidad de informaci6n de alta calidad para otras zonas geograficas del pais. Respecto de la informaci6n existente sobre taxonomfa y patrones de distribuci6n de especies a gran escala, existen importantes vacíos de informaci6n; no se esperan en el futuro grandes cam bios en el numero total de especies. Existen pocos estudios sobre patrones de distribuci6n de especies a gran escala, y más informaci6n es necesaria para identificar áreas de alta diversidad de especies, especialmente para algunos taxa, como tambien para identificar áreas que posean caracterfsticas unicas en relaci6n a especies (endemicas, especies claves) y a procesos ecosistemicos (disturbios, surgencias). Para la mayorfa de Ios invertebrados y macroalgas, !as áreas de alta diversidad de especies se encuentran en el sur de Chile. Nuevos estudios dirigidos a entender Ios factores que podrfan generar patrones a macroescala son necesarios, como tambien informaci6n sobre oceanograffa costera y disponibilidad de larvas. Esta informaci6n es clave para el disefio de una futura red de parques marinos. Por otro !ado, la informaci6n disponible sobre estructuras comunitarias y funcionamiento ecosistemico, especialmente sobre el efecto del impacto humano, provienen de pocas regiones geográficas. Mas informaci6n sobre otras zonas geográficas es requerida, particularmente si se consideran !as diferencias notables en temperatura, patrones de circulaci6n, heterogeneidad del habitat, y composici6n de especies, como tambien el efecto de surgencia y de El Nifio a lo largo de Ios más de 4.000 km de costa de Chile. Finalmente, listamos !as que consideramos son !as actividades humanas más dafiinas para el ambiente marino, e integramos esta informaci6n para sugerir posibles indicadores ambientales y necesidades basicas y sugerencias para conservaci6n marina in Chile.

Palabras clave: Chile, conservaci6n marina, patrones biogeográficos, estructura comunitaria, impacto humano.

INTRODUCTION history, and this single factor could have several effects (e.g., Valentine & Jablonski 1983). On the The profound influence of humans in marine sys- one hand, dispersal of early life history stages can tems has been recognized in the last few decades, occur over long distances, which could imply that and has been the major driving force behind the some marine species may be less vulnerable to creation of marine protected areas as a vehicle for extinction than terrestrial ones. On the other hand, marine conservation (Dayton et al. 1995, the use of different habitats during the life cycle Lubchenco et al. 1995, Allison et al. 1996). Ma- of marine species suggests that conservation ef- rine protected areas have increased dramatically forts directed at just one site may be ineffective over the last years in response to different objec- for population recovery. The differences in the tives, ranging from preservation of biodiversity, type, the scale, and the variability of the pro- protection of particular species, groups of species cesses affecting both systems suggest that the or critical areas (Norse 1993), to the prevention approaches developed for conservation of tern~s­ of overfishing (Davis 1989, Dugan & Davis 1993) trial ecosystems may very well fail in the marine and even enhancement of fisheries (Moreno et al. environments (Allison et al. 1998). 1984, Castilla & Duran 1985, Moreno et al. 1986, As in other developed and under developed Castilla & Bustamante 1989, Castilla & Fernandez countries, the establishment of parks and reserves 1998). However, the implementation of marine in Chile, as well as the biological basis for the reserves is relatively new, and the theoretical design of protected areas, is more advanced in basis for marine conservation is still poor in com- terrestrial than in marine environments parison with terrestrial ecosystems (Allison et al. (Ormazabal 1993). The majority of the popula- 1998). tion of Chile lives along its approximately 4200 Although it may be tempting to take advantage km of coastline, with most major cities located on of the experiences with reserve designs from ter- the coast. Moreover, Chile is one of the world restrial systems and apply them to the marine leading countries in exportation of fish products. environment, both systems differ dramatically Although the bulk of these landings consist of from minor to very fundamental factors. For in- pelagic resources, nearshore invertebrates and stance, while the greatest species diversity is algae have an important share and a dispropor- found on land, marine systems have a much greater tionately large economic and social impact since diversity at higher levels of organization (e.g., more than 30,000 fishermen are involved in the orders, phyla; Ray 1991 ), which implies a greater fishing activity (e.g., Bustamante & Castilla diversity of development and body plans as well 1987). Despite the enormous economic and social as evolutionary lineages. Marine organisms also significance of marine environments for the coun- exhibit a number of important differences in life try, the development of marine conservation pro- DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 799

grams and the scientific basis for sustainability view of the current knowledge about the ecolog) has not kept pace with the exploitation rate of and biogeography of the nearshore ecosystem in marine fisheries and the increasing use of the Chile, emphasizing new results not considered in coast for other purposes. Besides fishing, human previous reviews, and derive basic guidelines f01 impacts on the marine environment include coastal marine conservation. We emphasize patterns and aquaculture, species introductions, habitat alter- processes at meso- to large-spatial scales along ation and pollution related to human settlement the Chilean coast, although the majority of the and multiple activities, including those occurring information comes from local, within-site stud- far inland. The nature of human activity in the ies. Our goal is not to examine in detail differen1 marine and terrestrial environments differs, in- coastal systems but, based on the most relevan1 cluding the scale of its potential impact. Exploi- existing information, 1) to identify major biogeo- tation of marine resources takes place in open graphic and ecological features of nearshore eco- access areas, in contrast to privately owned lands systems and gaps in information, 2) to identify in terrestrial systems, triggering distinct behav- the most harmful human activities impacting the ioral and economic reactions. Most marine fish- structure and dynamics of these coastal systems, eries remove top predators, and secondarily her- and based on the above, and 3) to suggest the use bivores (Pauly et al. 1998), while herbivores are of indicators for the conservational status of dif- the main target in the exploitation of terrestrial ferent systems along the Chilean coast. Within systems (although not necessarily wild species). the continental shelf, we arbitrarily distinguished There is evidence that pollutants have more dra-. three major ecosystems: a) nearshore intertidal matic impacts on marine species than in terres- (rocky or sandy bottoms), ranging from the ex- trial ecosystems. These varied activities can have treme high water spring to the extreme low water important, diverse and yet unquantified effects spring; b) nearshore subtidal, ranging roughly on the marine ecosystem, affecting the bottom-up from the extreme spring low water to depths of and top-down regulation of the marine communi- about 30 m; and c) farshore subtidal, ranging ties, as well as altering natural habitats. from about 30 to 200 m in depth. We focused on While worldwide the effects of many human the first two ecosystems. Nearshore system (or activities have not been properly investigated, ecosystem), coastal system (or ecosystem) and Chile has been one of the pioneer countries in coastal environment were used indistinctly studies of human impact on marine communities throughout the manuscript to refer to intertidal (Moreno et al. 1984, Castilla & Dunin 1985, rocky shores, intertidal sandy bottoms, and shal- Oli va & Castilla 1986, Moreno et al. 1986, Castilla low subtidal areas. We first summarize the major & Bustamante 1989, Castilla 1999). The estab- physical and geographic features of the coast, lishment of two coastal marine reserves in Las localizing the distribution of major ecosystems Cruces and Mehufn evidenced the dramatic direct and known human impacted areas. Secondly, we and indirect effects of humans on invertebrate briefly describe large-scale, biogeographical pat- and macroalgal species (Moreno et al. 1984, terns and potential causal factors, to then concen- Castilla & Duran 1985, Oliva & Castilla 1986, trate on the structure and dynamics of local com- Moreno et al. 1986, Castilla & Bustamante 1989; munities for different habitats. Finally, we list there are no reports of long term monitoring pro- what we think are the most harmful human activi- grams in Montemar, Castilla 1996). These small ties by area and habitat along the coast, to then marine reserves (approximately 5 ha, Castilla integrate this information and suggest possible 1996) were not only key in demonstrating and indicators of human impact and basic needs for quantifying the nature and intensity of fishing on conservation. nearshore communities, but partly as a result of these "human-exclusion experiments", there is now a strong effort from some government agen- Main features of the Chilean coast cies directed at regulating management and ex- ploitation areas, and at the establishment of a The approximately 4,200 km of the Chilean con- network of marine protected areas in Chile tinental coast have a clear north-south orientation (Gonzalez et al. 1997). along the southeastern Pacific coast of South Although the establishment of any marine con- America, crossing different environmental con- servation policies along the vast coastline of Chile ditions strongly associated with latitude (from ea. must be based on a multitude of approaches and 18 to 56° S). Most of this coast occurs along the considerations, we think that scientific, biologi- subduction of the oceanic Nazca plate under the cal, and ecological principles should guide much continental South American plate. In this area, of the efforts. In this paper, we present an over- earthquakes of large magnitude are frequent, pro- 800 FERNANDEZ ET AL. ducing coastal uplifts or subsidences (Castilla Among the large-scale perturbations that affect 1988). Deep oceanic trenches and a narrow conti- the Chilean coast, the main oceanographic nental shelf are also characteristic features of the anomaly is the El Nifio event and its atmospheric area (Castilla & Oliva 1990). counterpart, the Southern Oscillation (ENSO; The Chilean continental shelf (up to a depth of Castilla et al. 1993). One of the prevailing inter- 2 200 m) covers a total surface of about 27,472 km , pretations is that ENSO events occur as an inter- with a mean width of about 6.54 km (Gallardo nal cycle of positive and negative feedback within 1984 ). This area has the following special charac- the coupled ocean-atmosphere climate system of teristics that influence nearshore ecosystem: (a) the tropical Pacific. Baroclinic equatorial Kelvin upwelled waters and abundant marine resources waves are generated and propagated eastward (ranked among the richest in the world; Arntz et toward South America, depressing the thermocline al. 1991), (b) particularly strong influence of and raising the sea level. The net result of this large-scale perturbations, such as El Nifio-South- event is an increase in surface seawater tempera- ern Oscillation (ENSO), (c) coseismic coastal ture of about 3-5° C and an increase in sea level of uplifts or subsidences due to earthquakes (Castilla up to 20 cm from Peru to Chile (Enfield 1989). et al. 1993), and (d) large areas of sea bottom Another large-scale perturbation is caused by exhibiting low oxygen availability (Fossing et al. periodic earthquakes. The coast of central Chile 1995). The relative importance of each event has been affected by large earthquakes at a regu- varies along the extended latitudinal gradient. lar period of 83 ± 9 years (mean ± SD; Comte et From an oceanographic point of view, several al. 1986), and many of them have produced im- circulation patterns have been proposed by dif- portant uplifts and subsidences of coastal rocks. ferent authors. A summary of the main oceano- These vertical uplifts translate into sea level graphic features has been presented by Castilla et changes for coastal benthic organisms, and the al. (1993) and Strub et al. (1998). The main cell of magnitude of these changes can be remarkable circulation is connected to the South Pacific anti- (Castilla 1988). cyclone gyre and driven by the West Wind Drift, According to Viviani (1979), the Andes Moun- which reaches the South American continent near tains, that run close and parallel all along the the 40-45° S and branches into two main current coast, create special climatic conditions. Four systems. The southern, poleward flowing branch distinct areas (Fig 1) can be identified along the is known as the Cape Horn system, and the north- Chilean coast (see Castilla et al. 1993): ern, equatorward flowing branch comprises what 1) Arid coast: This area extends from 18 to 27° is called the Humboldt or Chile-Peni Current S and is characterized by a northward-trending system (Fig. 1). As yet, most of the emphasis has cliff that is several hundred meters high in some been placed on the far shore oceanography. The areas (Araya-Vergara 1976). The land climate is geomorphological characteristics of the coastline defined as arid (Di Castri & Hajek 1976) or hy- and the little attention that nearshore oceanogra- perarid, but littoral zones and coastal waters are phy has received make difficult the assessment of not correspondingly warm because of coastal up- the influence of these two oceanic branches on welling. These upwelling processes weaken dur- coastal (few miles from shore) circulation. ing warm seasons of the year or warm periods One of the main oceanographic features of cen- such as the ENSO. Isotherms in surface water are tral and northern Chile is the upwelling of subsur- found nearly parallel to the coastline, ranging face waters into surface layers, which creates from about 16-20° C depending on the season of anomalous low temperatures and high productiv- the year and prevailing winds (Fig. 1; Viviani ity (Arntz et al. 1991, Strub et al. 1998). Along 1979, Santelices 1991). From a geomorphologi- the Chilean coast, there are numerous well-iden- cal point of view, this area shows an almost tified areas of up welling that together sustain one straight coastal rim with very few sheltered bays of the richest pelagic fisheries of the world (e.g., and no high-waterflow rivers reaching the ocean. Iquique, Coquimbo, Valparafso and Punta 2) Semiarid coast: This area extends from about Lavapie). The coastal upwelling systems that oc- 27 to 32° S, and is characterized by Plio-Quater- cur over 3,000 km along the continental shelf off nary marine terraces extending from the shoreline Southern Peru and North and Central Chile have to about 150-200 m offshore. According to Viviani a very high primary and secondary production (1979), in this area the climate is Mediterranean, (Arntz et al. 1991 ). In this area, the mineraliza- with rainfalls concentrated during the winter sea- tion of organic matter results in extensive oxygen son and increasing with latitude. There are clear depletion of the water column up to 60 m above seasonal trends in seawater temperature, but in 0 ° the sea floor, with temporal 2 variations be- general they are between 2 to 4 C lower than in tween 0 and 5 mM (Fossing et al. 1995). the arid area (Fig. 1; Robles et al. 1974). Numer- DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 801

ous upwelling zones exist along the coast (e.g., mostly during winter and with periods of drought Punta Lengua de Vaca, Curaumilla). This area during summer. Average seawater temperature also has an almost straight coastline with very shows a dramatic decrease in this area (Fig. 1). few sheltered bays or offshore islands and few There are many high-waterflow rivers (e.g., Bio- rivers reaching the sea (e.g., Limarf, Choapa, Bio, Cautfn, Tolten, Calle-Calle) reaching the Aconcagua). sea, and the oceanic temperate climate (Di Castri 3) Central coast: This area extends between & Hajek 1976) favors runoff erosion (and hence approximately 32° S and 42° S. The climate is sedimentation), particularly in winter. South of also Mediterranean, with rainfalls occurring 39° S there are many estuaries, which resulted

BIOGEOGRAPHIC GEOMORPHIC CURRENT PROVINCES &CLIMATIC SYSTEMS AREAS i ARID

COAST l ,I 1' 1' I PERUVIAN OR SEMIARID I CHILEAN COAST' 1'1 1'1 • 1- PROVINCE :!: z w ;" 11!: "" I 11!: I :;)::I! ~ /' l Uw CENTRAL ...... + 00 ~ ?7 COAST _.> 00 Ill ~ 71 :E ::;) J: + 1 t ~ .-;. t I ~ -? I I I ::!: ::!: 1- ~ z ' w "' 11!: "» ::l 11!: I FJORDS :;)::I! i Uw MAGELLANIC 1- .,. ... • COAST ZU) PROVINCE 11!:> 011) ;,a J: "' w D.. < 1 1 (.) Fig. 1. Schematic representation of the main structural features (biogeographic, geomorphic and climate, and current systems) of the Chilean continental coast (adapted from Castilla et al. 1993). Representaci6n esquematica de !as principales caracterfsticas de la costa de Chile continental (regiones biogeogr:ificas, clima y sistema de corrientes, adaptado de Castilla et al. 1993). 802 FERNANDEZ ET AL. from submergence by Holocene transgressions. 1997 and Prendergast et al. 1999 for a review). From a geomorphological point of view, this area Our goal in this section is to summarize the exist- is rougher than the previous one in terms of wave ing information on large-scale patterns of species impact and shows extensive beaches and dune distribution for different taxa, identifying areas fields. Sheltered bays are common, and Chiloe of high species diversity across taxonomic groups Island is the main coastal geomorphologic fea- and the possible causes generating these patterns. ture of the coastal area. Since most of these studies did not focus exclu- 4) Fjords coast: This area extends from about sively on the nearshore, it was not always pos- 43°30' to 56° Sand according to Pickard (1971), sible to separate the near from the farshore. We is one of the best examples of deep and rugged used mostly published studies, but also present fjord coasts in the world. The climate is oceanic unpublished data from the authors of this contri- with rainfall ranging between 2,000 and 3,000 bution, who will reveal details of those studies mm/year and homogeneously distributed through- elsewhere. Finally, we call attention to the major out the year. The shoreline is highly indented. In gaps in the existing information. this area the fjords penetrate inland through the The study of large-scale patterns of species glacially dissected Andes Range, and numerous distribution and ecosystem processes in Chile has short and low-waterflow rivers are found be- been limited to traditional biogeographical analy- tween 52° and 56° S. A strong and shallow ses. In these studies, discontinuities in composi- picnocline produced by a freshwater layer seetns tional affinities of the biota along geographic to characterize the water column within the fjords. gradients were used to determine biogeographic Average sea water temperature is the lowest of the provinces and infer probable causes for their bor- coast of Chile (Fig. 1). ders as well as the probable geographic origin of Tide ranges also vary along the coast of Chile, the species. Documentation of patterns at mesa- from semi-diurnal tides of 1.5-2 m amplitude scales (between the local-scale of experimental from Arica to Valdivia, to 8-14 m of amplitude studies and the continental scales of traditional between Puerto Montt and Punta Dungeness biogeographic analyses), are virtually non-exis- (Viviani 1979). In the fjords area tidal amplitude tent (but see Camus 1998, Brazeiro 1999, and varies between nearby locations. Other important below). The main reason for the lack of studies at factors that vary along the coast are related to the meso-scale is the scarcity of appropriate data- human settlement and activity, and are reported bases. For instance, while some information ex- below (Tables 3 and 4). ists about geographic ranges for a great number of species, sampling intensity and distribution along the coast is so scattered that it is not possible to Large-scale patterns of the biota and their poten­ examine latitudinal trends in diversity or site tial causal factors occupancy with more than ten degrees latitude of precision. Large-scale patterns of biotic and abiotic factors From a biogeographic point of view, the south- provide key information for identifying areas of eastern Pacific shelf area is within the so-called high species diversity as well as areas which Temperate Pacific Realm, which to the north bor- possess unique characteristics in terms of ecosys- ders the Panamic Province around Paita, in Peru tem processes (e.g., particular disturbance, up- (4-5 °S). The existent information about biogeo- welling regimes) and species (e.g., endemic spe- graphic provinces and compositional affinities cies, keystone species). This knowledge is essen- show different patterns for macro algae and benthic tial for the . identification and design of nature invertebrates within this realm (Viviani 1979, reserve networks. Since hot-spots of diversity, Castilla 1979, Santelices 1980, Brattstrom & rarity, endemic, and endangered species vary Johanssen 1983, Santelices & Marquet 1998, across taxonomic groups, as it has been shown by Lancellotti & Vasquez 1999). For benthic inver- studies in terrestrial taxa (Prendergast et al. tebrates, several studies have attempted a zoo- 1993, Dobson et al. 1997), no single area would geographic zonification of the coast based on the support all the processes and species important distribution of the species (e.g., provinces, tran- for conservation. Thus, the problem of identify- sition zones, borders; see below, Table 1; Dall ing and selecting areas for conservation usually 1909, Carcelles & Williamson 1951, Boltovskoy requires the application of area selection methods 1964, Stuardo 1964, Marincovich 1973, Knox that allow identification of a combination of char- 1960, Hartmann-Schroeder & Hartmann 1965, acteristics that would jointly maximize the pres- Dell1971, Smenov 1977, Viviani 1979, Sebens & ervation of species and ecosystem processes in Paine 1979, Brattstrom & Johanssen 1983, the long term (Pressey et al. 1993, see Csuti et al. Lancellotti & Vasquez 1999). Different taxa and DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 803

TABLE 1

Summary of the results of the three most recent studies about zoogeographic units and borders in Chilean waters. The total number of species included in each case, as well as the taxonomic groups considered are listed. The major biogeographic breaks in species distribution and the transition zones are included for both litoral ( < 50 m) and sublitoral environments (> 50 m). ND indicates no data

Resumen de Ios resultados de Ios tres estudios mas recientes sobre unidades zoogeognificas y sus lfmites en Chile. El numero total de especies inclufdas y Ios grupos taxon6micos considerados en cada caso son tambien listados. Los mayores quiebres biogeogr:ificos en la distribuci6n de especies y en las zonas de transici6n son listados separadamente para ambientes litorales ( < 50 m) y sublitorales (>50 m). ND indica que no hay datos disponibles

Publication Taxonomic Groups Analyzed Number Biogeographical and Transitional Regions of species Litoral Sublitoral

Viviani (1979) Cirripedia, Macrura. Brachyura, North: !2° S South: 41° S Anomura (Porcellanidae), South: 40-46° S (no clear break point, Polyplacophora, Bivalvia (Pelecypoda), 282 many small break points Asteriodea, Echinoidea, Holothuroidea; between 35-45) Bryozoa Actiniaria, Cirripedia, Macrura, North: 33° S North: 33° S Brattstrom and Brachyura, Anomura, Polyplacophora, South: 42° S South: 42° S Johanssen ( 1983) Gastropoda, Bivalvia, Asteriodea, 240 Transition 33-42° S Transition 33-42° S Ophiuroidea, Echinoidea, (42 strong breaks Holothuroidea, Ascidiacea 42-48 weak breaks) Porifera, Anthozoa, Polychaeta, Mollusca (Polyplacophora, Gastropoda, (< 100 m) Lancelloti and Vasquez Bivalvia), Crustacea (Cirripedia, 1,597 North: 18-35° S NO (1999) Amphipoda, Isopoda, Brachyura, Center: 35-48° S Anomura), Echinodermata (Asteriodea, South: 48° S Ophiuroidea, Echinoidea, Holothuroidea), Ascidiacea depth were considered in each of these studies is higher in deeper waters (Brattstrom & Johanssen (Table 1), and although they proposed different 1983). Subantartic species are found in the north biogeographic schemes, there are general coinci- only in deep waters. The taxonomic groups in- dences. First, there are two major biogeographic cluded in the analysis conducted by each author provinces (but see Lancellotti & V asquez 1999): may have also contributed to the small discrepan- (a) the Peni-Chile Province (from Paita in Peru to cies (see Table 1). Viviani (1979) suggested a Valparafso in Chile) and (b) the Magellanic Prov- clear asymmetry in the latitudinal distribution of ince (Chiloe, Island to cape Horn). The exact different taxonomic groups (see also Brattstrtim latitude of each province varies up to 2-3 degrees & Johanssen 1983). Thus, the use of different among the different authors. Secondly, most au- taxonomic groups in a pool of species classified thors recognized a more diffuse 'transition zone' only by depth could produce different outcomes. in central Chile, from around Valparafso down to Independent analyses by taxonomic group could Chiloe Island. determine if the discontinuities in compositional Differences among studies can be partly due to affinities of the biota along geographic gradients the species included and the ranges of depth dis- are consistent among taxa, and also if the same tribution used in each analysis. In general, shal- causes could affect in similar ways the different low water species have been analyzed separately taxa. For instance, the distribution of isopod and from deep-water species (but see Table 1), and amphipod species (not used by Viviani 1979 and the effect of this factor can be easily observed. Brattstrtim & Johanssen 1983) could have af- The biogeographic break at 42° S is stronger for fected the determination of the discontinuity at shallow than for deep-water species (Brattstrtim 48° S recently suggested by Lancellotti & Vasquez & Johanssen 1983). Also, the number of species ( 1999). Both groups show high number of species with northern origin is higher in shallow waters and a discontinuity between 45 and 50° S. The while the number of species with southern origin pattern of species distribution may continue 804 FERNANDEZ ET AL. changing slightly as distribution ranges are modi- marine invertebrates is critical, and although simi- fied (when less studied regions, or deeper waters lar causes could explain the distribution of sev- are better known). eral taxa, some may be taxa specific. The general Circulation patterns, heterogeneity of the coast, pattern suggests that there is a "diversity hot- salinity, temperature, and tidal amplitude are some spot" in southern Chile (South of 42° S ), al- of the factors consistently mentioned to explain though we think that it does not occur for all the distribution of species along the coast of invertebrate taxa (e.g., Brachyuran, Anomuran). Chile. Large changes in patterns of water circula- The biogeographic analysis of the marine flora tion in the southeastern Pacific correspond re- of the Chilean Pacific coast shows a different markably with the most critical biogeographic pattern than for marine invertebrates. One area of boundaries around Paita and Tumbes in Peru and species affinity is found from the Magallan Strait the Chiloe Island in Chile (Fig. 1 ), giving support to Cape Horn (54-55° S), composed of mostly to this factor. Ongoing studies show that the total subantartic and endemic species, many with re- number of mollusk species increases towards high stricted distribution. A second, broader area ex- latitudes and the mean latitudinal range of the tends between 5 and 53° S and shows many en- species decreases in accordance with Rapoport's demic species, several bipolar species, and a Rule (Valdovinos, Navarrete & Marquet, unpub- gradual northward decrease in the number of ant- lished data). No effect of temperature was found arctic species. Within this region, a small discon- to explain the increase in mollusk species rich- tinuity is observed at 30° S (probably related to ness at high latitudes (Roy et al. 1998), and in- upwelling events, Santelices 1980). Santelices stead a strong correlation between number of (1980) hypothesized different distribution cen- species and heterogeneity of the coast was de- ters may have generated the current pattern. The tected (Valdovinos, Navarrete & Marquet, un- outstanding phytogeographic features of this re- published data). Another factor that may also be gion seem to be the high degree of endemism important in explaining the distribution of marine (32.3%), the strong influence of subantartic spe- invertebrates is the distribution of reproductive cies (34.4% ), and probably as a consequence, the and developmental modes of the different taxo- decrease in species richness towards the equator nomic groups along the latitudinal gradient. How- (Santelices 1980). Other species of macroalgae ever, information about modes of development are widely distributed (22.8%), bipolar (7.1 %) or and length of planktonic time is poor for most tropical (3.4%). In a recent paper, Santelices & taxa in comparison with other geographic areas of Marquet (1998) described the latitudinal varia- the world (Table 2). The identification of causal tion in species richness and geographic range size factors to explain the patterns of distribution of for 380 marine benthic algae along the coastline

TABLE2

Percentage of the total number of described species within a given taxonomic group for which exist information in our databases on body size, developmental mode (eg. brooders, broadcasters), larval type (lecitotrophic or planktotrophic), duration of plantonic life, and geographic ranges of species distribution. For comparison, we included within brackets the information available (also in %) for developmental modes for invertebrates along the coast of California (except for Crustaceans)

Porcentaje del total de especies descritas por cada grupo taxon6mico para !as cuales existe informaci6n en nuestra base de datos sobre tamafio corporal, modo de desarrollo (incubadores o dispersores), tipo de larva (lecitotr6fica o planctotr6fica), duraci6n del tiempo de vida planct6nico, y rango de distribuci6n geografica de !as especies. A modo comparativo, se incluye entre parentesis la informaci6n disponible (tambien en porcentajes) para Ios modos de desarrollo de Ios invertebrados a lo largo de la costa de California (excepto para Crustaceos)

Taxa Size Developmental Mode Larval Type Planktonic life Distribution

Gastropoda 80.5 35.5 (85) 11.6 8.3 94.5 Bivalvia 87.6 28.0 (34) 14.0 8.5 . 98.8 Polyplacophora 83.2 58.9 (50) 39.3 1.8 100.0 Echinodermata 86.8 56.6 (79) 25.0 21.1 94.7 Brachyura 100.0 100.0 100.0 16.2 100.0 Isopoda 49.0 100.0 100.0 1.0 100.0 Anomura 94.9 100.0 100.0 8.5 100.0 DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 805

of Peru and Chile (latitude l0° to 55° S), and than 8 to 10 species in the fjord area (Moreno & showed that the number of species increases with J ara 1984 ). As yet, the information available on latitude from about 20 at latitude 5° S to more distribution of fish species is restricted to inter- than 130 at latitude 55° S. This "anomalous" tidal and shallow subtidal fishes (Ojeda et al. in latitudinal species diversity pattern has also been press). reported for the Pacific coast of North America Latitudinal distribution of native species of (Gaines & Lubchenco 1982). The pattern is asso- birds, mammals, and reptiles associated to littoral ciated with a progressive decline in species mean environments along the Chilean coast are cur- latitudinal range size as diversity increases, fol- rently being investigated (Silva & Marquet un- lowing the Rapoport's Rule (Stevens 1989, 1996). published data). Using published records these As reported above, the same pattern seems to authors obtained distributional data for 93 spe- occur for marine invertebrates (Valdovinos, cies of birds, 25 mammals, and 14 reptiles regis- Navarrete & Marquet, unpublished data). Hot- tered as resident or occasional on the coast of spots of diversity of marine invertebrates (pool- Chile (no more than lO km offshore). The general ing Gastropoda, Bivalvia, Placophora, Echino- latitudinal pattern in species diversity (all taxa dermata, Isopoda, Anomuran and Brachyuran) pooled) is non-linear. Total species richness in- and macroalgae are found south of 50° S (>897 creases with increasing latitude between 18 and species), between 35 and 40° S (819-896 spe- 28° S and south of 50° S, but from 28° S the cies), and between 25 and 30° Sand 40 and 50° S number of species decreases dramatically as lati- (748-818 species). tude increases to 50°S. The highest species rich- Large scale biogeographic analysis of coastal ness occurs between 25° and 30°S corresponding fish species are lacking, but ongoing studies show to the coastal area between Paposo and La Serena, that coastal fishes assemblages of littoral marine where the number of species was as high as 80. fishes also exhibit important compositional breaks In general, latitudinal patterns in diversity vary around 40-42°S, but in this case, diversity de- among these taxa. Mammals show an increase in creases toward higher latitudes (Ojeda et. al. in number of species with latitude, from 5 species press). The intertidal fish fauna of northern Chile around 20° Sup to 19 species around 55° S, while is relatively poor, with no more than 6 to 7 species reptiles species richness decreases progressively in Antofagasta (23° S; Ojeda, unpublished data). as latitude increases, from 8 species between 22° This fish assemblage is conformed by a subset of and 30°S to one species south of latitude 41 o. the species also found along the central Chilean Birds, on the other hand, show a more complex coast (ea. 33° S), including the kyphosids Graus latitudinal richness pattern with several peaks nigra and Girella laevifrons and the blenioid and troughs. Richness reaches a peak of 65 spe- Scartichthys viridis. Rocky intertidal fish fauna cies in north/central Chile, between 25° to 30° S. of central Chile (30- 33° S) is fairly diverse with From this latitude to the south, richness decreases 18 to 20 species (Varas & Ojeda 1990, Mufioz & (33 species) until around 50° S and tends to Ojeda 1997). This assemblage is composed of increase further south. The latitudinal pattern in resident species (Blenniidae, Tripterygiidae, and threatened species (vulnerable or endangered) Clinidae) and transient or temporary species that shows also a non-linear pattern. It remains rela- inhabit the intertidal pools as juveniles (e.g., tively high(> 10 species) in north/central Chile Kyphosidae; Varas & Ojeda 1990). South of with a major peak of 13 species at around lati- Maiquillahue Bay (39°S), intertidal fishes in pools tudes 35°- 40° S. Endemicity peaks at around . are scarce and only some clinids and blennids latitude 30° S (5 reptile species). There are no remain, being Calliclinus geniguttatus the most endemic birds and only one endemic mammal conspicuous. Myxodes virides, Tripterygion species. The conservation status of seabirds as cunninghami and Scartichthys viridis are also well as the identification of marine birds and found in the rocky areas of the exposed Pacific mammals included in International Conventions coast down to Chiloe Island. In the area of Valdivia have been discussed by Schlatter (1984) and tide pool fishes of the Nototheniidae family, an Schlatter and Hucke-Gaete (1999) respectively. abundant group in the southern channel region In an additional study, Schlatter and Simeoni south of 45 °, start to appear in intertidal pools. ( 1999) recognized 109 species of marine birds The more emblematic species in the intertidal associated to oceanic and costal areas in conti- habitats of the southern fjords south of 45° are the nental and insular Chile. Out of this total, 23 nototheniiforms Harpagifer bispinis and species ( =21%) are included in some threat cat- Patagonothoten cornucola, together with the egory. zoarcid Austrolychus deprecisseps. The local in- These studies run short in term of representing tertidal fish assemblages do not contain more the species diversity inhabiting coastal and 806 FERNANDEZ ET AL. subtidal environments in Chile. Without doubt Intertidal and shallow subtidal rocky habitats the total number of species, a large fraction of which are endemic, is substantial (specially to- Wave exposed rocky intertidal areas are common wards subantartic areas, Viviani 1979, Santelices habitats all along the Chilean coastline. In these & Marquet 1998), as large as it is our current lack systems the basic taxonomy of macroinvertebrates of knowledge of their conservation status and the and macroalgae is generally well known. More need for a national system of Marine Protected intensive samplings and taxonomic and molecu- Areas. lar work should turn up new species and clarify the status of many others, but no big changes in the total number of species are expected. There Patterns of community structure and processes are some fairly ·specious groups of intertidal in- affecting nearshore communities vertebrates whose taxonomic identification is particularly difficult and need revision, such as The study of biological and physical processes limpets of the genera Lottia, Scurria, Collisella structuring communities at one or a few sites has and Nacella, and amphipods in general. A recent been the main focus of ecological research in book about taxonomic identification of Chile. Over the past two decades these findings macroalgae has helped clarify the status of inter- have reached recognition as one of the best stud- tidal and shallow subtidal algal groups in central ied marine systems of the world, and examples of Chile (Hoffman & Santelices 1997). No equiva- Chilean studies are starting to appear in basic lent exists for invertebrates. As for most ecologi- ecological textbooks (e.g., Giller 1984, Putman cal systems, it is difficult to determine the exact 1994, Paine 1994, Raffaelli & Hawkins 1996, number of species that coexist in the intertidal Barnes & Hughes 1999). However, this informa- zone. Local communities at exposed-rocky benches tion comes from a relatively small number of in central Chile are composed by some 30 to 60 study sites, and is mostly restricted to the inter- macroscopic invertebrate species, both sessile tidal zone. Recent reviews summarized much of and mobile (e.g., Marquet et al. 1990). This num- the information available and presented the cur- ber does not consider the small sized species that rent view of our understanding about the dynam- inhabit almost exclusively within the mussel bed ics of Chilean benthic nearshore systems (e.g., matrix or inside kelp holdfasts (Cancino & Santelices 1989, 1990, Castilla & Paine 1987, Santelices 1984, V asquez, unpublished data, see Vasquez & Buschman 1997, Castilla et al. 1993, below). Between 40 and 60 macroalgal species MacLachlan & Jaramillo 1995). In this section, can be found in a given site, not taking into we draw from these reviews and other basic stud- account microscopic forms or epiphytes (Camus ies to present what we believe are the most impor- 1998, Broitman and Navarrete, unpublished data). tant patterns and processes in the different sys- A fairly diverse assemblage of tidepool fishes tems. Our goal is twofold. First, whenever pos- conformed by 10 and up to 18 species is present at sible we want to identify key species and pro- many sites in central Chile (Mufioz & Ojeda 1997). cesses that for their impact on the rest of the There is no information about latitudinal trends community need special attention in conservation in species richness of local communities. plans, and which could be used as indicators of Zonation patterns have been extensively de- the degree of intervention of the system. Sec- scribed for various localities (e.g., Alveal 1971, ondly, we want to call attention to the major gaps Santelices et al. 1977, Castilla 1981 ), most of in information in the different habitats, which them heavily affected by human collection. From either make it impossible to identify key compo- Chiloe Island (ea. 43 o S) towards the north, the nents in the local system, or jeopardize the appli- kelp Lessonia nigrescens forms a characteristic cability of the ones we do identify as such. belt at the lower end of the intertidal zone. Among In Chile there are two major and clear biases in the holdfasts of the large kelps there is either the amount and intensity of the existent ecologi- patches of algal turfs, mostly Gelidium spp. and cal information. First, most of the experimental other branched corticated algae, or patches of work has been conducted on rocky and sandy fleshy and calcified crustose algae. On rocky intertidal zones, or shallow rocky subtidal habi- benches not directly exposed to breaking waves, tats. Secondly, the great majority of the ecologi- the mosaic of algal turf and crustose algae· can cal ·studies have been conducted on a relatively cover extensive areas of the low and mid-low small fraction of the coast, between about 30 and intertidal zones. Along most of its range, from 39o S (Santelices 1990, Camus 1998). Thus, our central Chile (about 30° S) to Magellan Strait, account of the different systems is tainted by Lessonia shares the low intertidal zone with the these limitations. bull kelp, Durvillaea antarctica. This latter spe- DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 807 cies is more prevalent to the south, and in areas terns described above can be substantially modi- south of Valdivia is relatively protected from fied, directly or indirectly, by fishing. For in- human exploitation extending up into mid and stance, removal by humans of the muricid gastro- even high intertidal zones. South of Chiloe, o'n pod Concholepas concholepas allows mussel beds the open coast of the fjords region, the scarce to extend into the lower intertidal zone (Dunin information available indicates that Durvillaea is &Castilla 1989), and removal of large keyhole relatively more abundant and prevalent than limpets produces the extension of Mazzaella Lessonia (Dayton 1985). At about 20° S, Lessonia laminarioides well into the low intertidal (Moreno reaches its northernmost limit and the substratum & Jaramillo 1983). is occupied mostly by encrusting coralline algal Based on the work conducted in the region forms and high densities of herbivores. The mid between 32 and 36°S, and around 39°S, it is pos- intertidal zone of most sites in central and south- sible to identify critical species and processes in ern Chile, south of about 32° S, is dominated by the intertidal system. First, there are two func- beds of the mussel Perumytilus purpuratus tional groups of overriding importance as spe- (Castilla 1981). At some sites and on a more cies-engineers (Jones et al. 1994), which provide seasonal basis, a mixed mussel bed of P. structural habitat for other species. In the mid purpuratus and Semimytilus algosus can extend intertidal zone, mussel beds (mostly Perumytilus down to the low intertidal zone and occupy the purpuratus) provide a microhabitat for a large space among Lessonia plants, temporarily over- number of small sized species which are found growing the Gelidium spp. turf. When mussel only within the mussel bed matrix, as well as for beds are absent from the mid zone, the substratum species that are found elsewhere but either find is occupied by chthamaloid barnacles and refuge or recruitment sites in the mussel bed corticated foliose algae (mostly Mazzaella (Cancino & Santelices 1984, Castilla et al. 1989, laminariodes) and fleshy crustose algae (largely Navarrete & Castilla 1990, Alvarado & Castilla Hildenbrandtia spp. in central Chile and Ralfsia 1996). These beds can cover more than 80% of the spp. in the South). In the mid zone of exposed substratum at these tidal elevations and experi- fronts of Chiloe Island and in the low intertidal ments have demonstrated that they are the domi- zone of semi protected fronts, it is frequent to find nant competitors for space (Paine et al. 1985). juveniles and adults of Austromegabalanus However, experiments have also demonstrated psittacus (a large size barnacle) together with that, partly as a result of mussel larvae being high densities of the muricid Concholepas unable to settle directly onto bare rock (Navarrete concholepas. While in tidepools and channels of & Castilla 1993), the beds are very slow to re- central Chile the black sea urchin, Tetrapygus cover from disturbance, particularly in the ab- niger, is probably the most important browser sence of recruitment mediators. A different pat- species, south of 39° S the only sea urchin present tern was found in southern Chile, where the re- in the emergent substratum and intertidal pools is covery rate of Perumytilus purpuratus was very the red Loxechinus albus, which coexists with the fast when herbivores and carnivores were ex- former one in central Chile (Contreras & Castilla cluded (Moreno et al. 1986). After the experi- 1987, More no & Vega 1988). mental exclusion of herbivores (Fissurella picta), North of about 32° S, .where mussel beds are Perumytilus recruited at increasing rates during 2 scarce, the mid zone is dominated by ephemeral years, generating a matrix that facilitated mussel algae (generaPorphyra, Enteromorpha and Ulva), larval settlement. Thus, mussel beds in Central fleshy crustose algae (mostly Hildenbrandtia) Chile are particularly sensitive to disturbance, and bare rock. Mussel beds appear again as domi- while in southern Chile the response may be nant components of the mid zone at some sites different depending on the species that are simul- north of about 20°S and up to subtropical areas in taneously disturbed. Peru. On the shaded, more protected side of ver- The other important structural components in tical walls the crustose alga Codium dimorphum, the low, rocky intertidal zone are the large kelps, a thick and soft fleshy crust, can cover large areas Lessonia nigrescens and Durvillaea antarctica. of the mid intertidal landscape (Santelices et al. These algae play two important roles as species- 1981 ). The high intertidal zone throughout the engineers. First because of their size and strong Chilean coast, down to the open coast of the stipes, the plants create a special regime of physi- Magellan region, is characterized by a band of the cal disturbance, which is sufficient to prevent ac- chthamaloid barnacles Nothochthamalus cess from large herbivores (e.g., sea urchins) into scabrosus and Jehlius cirratus and the seasonal the low and mid-low intertidal zones (Ojeda & appearance of ephemeral algae. Experimental Santelices 1984) and can substantially modify the evidence has shown that general zonation pat- water flow and wave forces for other algal and 808 FERNANDEZ ET AL.

invertebrate species that inhabit among the plants. in barnacle and ephemeral algal cover (Paine et Secondly, the holdfasts of these kelps, particularly al. 1985). This species can remove and consume Lessonia (see below), serve as a microhabitat to a several mussels at once, creating gaps in the large number of invertebrate species, many of mussel beds that can persist for months or years. which are rarely found in open areas (Cancino & Second, the exclusion of humans from a stretch of Santelices 1984, V asquez unpublished data). Be- the coast (see below) revealed that the edible sides mussels and kelps that are found along most muricid gastropod Concholepas concholepas, of the coast of Chile, a special situation occurs which is kept at low densities by human collec- within the Antofagasta Bay in northern Chile, where tion in open (unprotected) areas, can completely a dense bed of the giant tunicate, Pyura praeputialis decimate the mussel beds from the low, mid and monopolizes large areas of the mid and low inter- even mid-high intertidal zones (Castilla & Duran tidal zones (Clarke et al. 1999, Guifiez & Castilla 1985, Moreno et al. 1986, Duran & Castilla 1989, in press). These beds also serve as a microhabitat Castilla 1999). Because the dominant intertidal to a large number of species, not commonly found mussel in these beds, P. purpuratus, does not elsewhere (Paine & Suchaneck 1983). reach more than three to four cm in length, mus- Several strong biological processes have been sels cannot find a refuge in size from either determined and experimentally quantified at sites Heliaster or Concholepas. It is not clear how in central Chile (33 °S) and around the area of strong are the direct and indirect interactions Valdivia ( 41 °S). As in many other coasts of the between these two predators, but certainly the world, top-down (trophic) factors play a major strength should be modulated by the intensity of role in the regulation of local intertidal communi- human collection of the gastropod. In the area of ties in Chile. Probably the strongest top-down Valdivia, 840 km to the south, a comparable force in these ecosystems is the intense human human exclusion experiment als.o showed that collection of invertebrates, algae and fish that can Concholepas can dramatically reduce the abun- profoundly transform the landscape (Castilla et dance of mussel beds, freeing space for other al. 1994, Branch & Moreno 1994, Castilla 1999). sessile species and triggering several indirect ef- We will treat human impacts separately in the fects at different trophic levels (Moreno et al. next section and will concern ourselves here with 1986, Godoy & Moreno 1989). At these sites, the more 'naturally intertidal' interacting spe- there are no Heliaster, whose geographic distri- cies. There is a diverse arrange of vertebrate and bution does not extend much beyond 36° S, and invertebrate carnivore predators that feed on both no other sea star seems to compensate for its mobile and sessile invertebrates (Castilla 1981, predation pressure in the mid zone. The crabs of Castilla & Paine 1987, Navarrete & Castilla 1993, the genus Acanthocyclus can be very abundant at Branch & Moreno 1994, Mufioz & Ojeda 1997). some sites in central and southern Chile (N avarrete Separate experiments have shown that many of & Castilla 1988, 1990) and their community-wide these predators can have important effects on effect has yet to be quantified. In relatively wave- different prey populations, but so far there has protected areas, the muricid predatory gastropod, been no experiments designed to quantify their Acanthina unicornis (= Nucella calcar) has been effects in a comparable fashion (e.g., Navarrete & shown to heavily prey on mussel populations at Menge 1996, Berlow et al. 1999). However, from mid-low intertidal levels, but they do not seem to the isolated studies it is now very clear that dif- be able to persistently control their tidal distribu- ferent species have very different impacts at the tion (Moreno 1995). At the moment we cannot community level, suggesting a pattern more alike determine how much the impacts of Concholepas to a keystone type of predation than diffuse pre- and Heliaster change north of about 32° S and dation (e.g., Menge et all994, Navarrete & Menge south of Chiloe Island. Preliminary evidence for 1996, Robles & Robb 1993). This means that it is northern Chile does suggest that the overall im- possible to identify one or a small subset of pact of predation on major patterns of community species within the predatory guild, which have structure might be very different to that in central disproportionately strong effects on some com- Chile (Camus 1998). Recent studies by V asquez munity variable (Power et al. 1996, Allison et al. et al. (1998) suggest that large-scale interannual 1996). In central Chile, there are two carnivore perturbations, namely El Nifio events, can have species that appear to have a much stronger per strong effects on local community dynamics and capita effect than the rest of the carnivores with might modulate other biological interactions in which they coexist. First, experimental removals northern Chile. of the sun star Heliaster helianthus from the mid Regulatory top-down forces are not restricted to intertidal zone led to a large reduction in the high trophic level predators. Experimental ma- cover of mussel beds and a concomitant increase nipulations have shown that herbivores can con- DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 809 trol zonation patterns of macroalgae in the mid and pattern is observed even at areas with low densi- low intertidal zones. In the low zone of central ties of sea urchins and other herbivorous inverte- Chile, the balance between the algal turf and crus- brates. Recent experiments suggest that the cul- to se (fleshy and calcareous) algae seems 'to be prit for this pattern is the blennioid fish Scartichtys determined by herbivory (Ojeda & Santelices 1984, viridis, which plays an important role in main- Santelices 1990). In turn, the abundance of herbi- taining the low abundance of foliose macroalgae vores is regulated to some extent by the whiplash and the relatively high cover of brown and red effect of the large Lessonia plants. In relatively crustose algae (Ojeda & Mufioz 1999). Rocky wave-protected channels and tidepools where intertidal fishes of central Chile forage on a wide Lessonia is naturally absent, herbivores reach high variety of species, including sessile and slow- densities (particularly the black sea urchin moving (e.g., macroalgae, barnacle and gastro- Tetrapygus niger), and a blanket of pinkish calcar- pods) and active animals (e.g., decapods, iso- eous algae (Mesophyllum) covers the low zone and pods, amphipods, and small fishes). The inter- extends into shallow subtidal areas (Santelices tidal fish assemblage is composed of three trophic 1990). In exposed benches there is a diverse guild groups: one guild consisting of five species of of herbivores, including several large chitons, key- carnivorous (Bovichthys chilensis, Gobiesox hole limpets, sea urchins and herbivorous fish, but marmoratus, Auchenionchus variolosus, A. we have no information about their relative im- microcirrhis and Graus nigra), a second guild of pacts. Herbivory is also intense at mid tidal eleva- three species of microcarnivorous (Myxodes tions. The most abundant key-hole limpets are viridis, Tripterygion cunninghami, and T. Fissurella crassa and F. limbata in central Chile, chilensis), and a third guild of two species (the and F. picta, also followed by F. limbata, in south- omnivore Girella laevifrons and the herbivore ern Chile. Experimental manipulations in the Scartichthys viridis; Mufioz & Ojeda 1997). Valdivia area showed that key-hole limpets can In Chile, the systematic study of recruitment control the presence of the mid-intertidal belt of (supply-side) as a factor structuring local, rocky the alga Mazzaella laminarioides (Jara & Moreno shore communities is only beginning (e.g., Moreno 1984, Moreno et al. 1984 ). In central and northern et al. 1993, Gallardo et al. 1994, Carrasco & Chile the Fissurella species are the largest herbi- Carvajal 1996, Cafiete et al. 1996). This situation vores and probably the most efficient mid littoral holds also for other habitat types (e.g., sandy consumers (Oliva & Castilla 1986). Other species beaches, see below). We have virtually no infor- of limpets, Siphonaria lessoni and Collisella spp., mation about the kinds of processes that regulate are also found in the same habitat. These two recruitment rates of any species along the coast, species of limpets have small size, and exhibit including the commercially exploited ones. Nor do changes in individual growth rate and in their we know if there are gradients of recruitment along distribution pattern when Fisurella spp. is present the more than 4,000 km of open coast, or if particu- (Godoy & Moreno 1989). Again, these key-hole lar sites could be classified as sources or sinks in limpets are heavily exploited by humans, so their terms of the population dynamics of some species: community-wide effects became apparent only after This information is critical in the design of marine excluding humans from a stretch of the coast. The reserve networks (Roberts 1998). Similarly, the same key-hole limpets appear to have comparable relative importance ofbottom-up processes in struc- effects in central Chile (Oliva & Castilla 1986). In turing the marine communities in the nearshore is southern Chile, there is also one herbivorous gas- lacking. Recently, V asquez et al. (1998) docu- tropod that can play an important role in commu- mented that the frequency of upwelling appears nity structure, the snail Tegula atra. This snail eats not to be a determining factor of the diversity only filamentous ephemeral algae and ulvoids, and (species richness) of rocky littoral communities in its vertical distribution tracks the abundance of northern Chile. Some general ideas about major this type of algae at mid and low intertidal zones, oceanographic processes affecting nutrient supply as well as the shallow subtidal, where it can clean to the coastal areas, or driving recruitment, as well the rocks of the turf of ephemerals. This facilitates as quantitative information on recruitment rates the seasonal recolonization of the low intertidal along large stretches of the coast is urgently needed. and very shallow subtidal areas by Macrocystes pyrifera (Moreno & Sutherland 1982). A typical landscape at low and mid intertidal Intertidal, soft-bottom habitats levels in channels not directly exposed to break- ing waves is the dominance of Hildenbrandtia Besides the common rocky intertidal areas, sandy spp. and other fleshy crustose algae with sparse beaches are common features along the Chilean barnacles and other sessile invertebrates. This coast, between Arica (ea. 19° S) and the exposed 810 FERNANDEZ ET AL.

coast of Chiloe Island (ea. 42° S). Microtidal Jaramillo 1982, 1987b, Varela 1983) could ex- estuaries (1-2 m of tidal range) are also repre- plain the differences in species richness of sented, but only along the coast of south central peracarids along the Chilean coast. The influence 1 Chile (ea. 35-41 o S; Pi no 1994 ). Similarly, and of subantarctic waters on sandy beaches located even when salt marshes are found along the entire in southern Chile may also explain the better Chilean coast, they are more abundant at south representation of valviferan species of central Chile. In the northern region, marshes Macrociridothea, a typical taxon widely distrib- occur primarily at areas located close to river uted on the southern tip of South America (cf. outlets; further south (ea. 41-43° S), they also Moreira 1973). Recently, Brazeiro ( 1999) dis- occur in inland marine waters such as that of the cussed patterns of community structure and dis- archipelagos. Most of the faunistic studies car- tribution of the Chilean sandy beach macroinfauna ried out in sandy beaches and intertidal estuarine and found that species with the widest range of flats deal primarily with benthic macroinfauna distribution tend to be the most abundant. (J aramillo 1978, 1982, 1987a and b), although In estuarine areas the macrofauna is dominated local studies of the meiofauna inhabiting the very by different taxonomic groups in the upper (i.e., shallow sediments (about 1 cm deep) have been close to the limnetic areas) and middle reaches, as done (Clasing 1976). well as in the outlets (i.e., closest to the marine Studies on the latitudinal distribution of spe- environment). The typical estuarine taxonomic cies and abundance of the macroinfauna inhabit- groups in the upper reaches are Insecta (Diptera, ing sandy beaches showed that peracarids (prima- Coleptera, Trichoptera, among others) and rily cirolanid isopods, Excirolana spp.) are domi- Oligochaeta (Naididae, Tubificidae; cf. Garcfa & nant, in terms of species richness. The cirolanid Ojeda 1995). Polychaetes, followed by amphi- isopod Excirolana hirsuticauda and the anomuran pods, are the dominant groups in the middle crab Emerita analoga are usually the most abun- reaches (the most common species are Prionospio dant taxa, being this crab the main contributor to (Minuspio) patagonica, Capitella capitata, intertidal biomass (Sanchez et al. 1982, Jaramillo Perinereis gualpensis and the amphipod 1978, 1982, 1987b, 1994, Jaramillo et al. 1998, Paracorophium hartmannorum; Jaramillo et al. Brazeiro et al. 1998). Studies carried out at dif- 1985, Quij6n & Jaramillo 1993). At the estuarine ferent latitudes showed that the lower shore lev- outlets the macroinfauna is dominated by poly- els are usually occupied by E. analoga all along chaetes (e.g., Euzonus heterocirrus), peracarid the Chilean coast. However, latitudinal changes crustaceans (Excirolana hirsuticauda, E. monodi in species composition are commonly observed at and Macrochiridothea mehuinensis) and bivalves the upper intertidal zone (dry zone and drift line; (juveniles of Mesodesma donacium; Jaramillo et Cas till a et al. 1977, Hernandez et al. 1998, al. 1985). Latitudinal analyses of intertidal estua- J aramillo 1987b, 1994 ). While the ghost crab rine macroinfauna, as those cited above for the Ocypode gaudichaudii and the cirolanid isopod sandy beach macroinfauna, have not yet been Excirolana braziliensis are commonly found in conducted. There are not many studies on other the upper shore levels of northern Chile (ea. 19- biotic components of soft habitats such as 230 S), the talitrid amphipod Orchestoidea meiofauna and salt marsh plants. The meiofauna tuberculata, the tylid isopod Tylos spinulosus inhabiting very shallow sediments (about 10 mm and E. braziliensis are found in similar levels at deep) in mud flats near Puerto Montt (ea. 41° S) north central Chile (ea. 28-30° S). On the other was dominated by nematodes followed by ostra- hand, 0. tuberculata and E. braziliensis are typi- cods and harpacticoid copepods (Clasing 1976). cal inhabitants of sandy beaches of central and More than 60 species of vascular plants have been south central Chile (ea. 33"42° S). These studies found in these habitats; Sarcocornia fruticosa also showed that the number of species of isopods and Anagallis alternifolia are the most frequent, (Excirolana and Macrochiridothea) is higher at while Spartina densiflora is common in marshes sandy beaches located in south central Chile (ea. of south central Chile (San Martin et al. 1992, 40° S; Jaramillo 1982, Jaramillo 1987b). A higher Ramfrez et al. 1990). number of taxonomic and ecological surveys car- Patterns of macroinfaunal communities inhab- ried out in sandy beaches of southern Chile (e.g., iting exposed sandy beaches of the Chilean coast have been associated to spatial and temporal vari- ability of single physical factors such as mean Pino M (1994) Geomorfologfa, sedimentologfa y grain size and water content of sands (J aramillo dimimica de la circulaci6n en estuarios micromareales 1987a, Jaramillo et al. 1996, Hernandez et al. del centro sur de Chile. Resumen XIV Jornadas de 1998) and to a composite index, the Dean's pa- Ciencias del mar, Puerto Montt, Chile: 106-107. rameter, which describes the morphodynamic DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 811 beach type (Jaramillo & McLachlan 1993, significant increase in the abundance of the most Jaramillo et al. 1998). In south central Chile, abundant species of the intertidal macroinfauna species richness, abundance and biomass of the of the Queule river estuary (the polychaete macroinfauna increases from reflective to dissi- Prionospio ( Minuspio) patagonica), when experi- pative beaches (Jaramillo & McLachlan 1993). mental areas were protected from predation by Similar results were found in sandy beaches of crabs, fishes and birds. Similarly, Vehisquez north and north central Chile (Jaramillo et al. ( 1987) found that the whimbrel Numenius 1998). These results suggest that similar factors phaeopus affects the population structure of its (i.e., beach morphodynamics) might control the major prey, the polychaete Perinereis gualpensis community structure of the Chilean macroinfauna, Jeldes. The largest worms inhabit deeper sedi- independent of geographic latitudes. However, ment layers, escaping predation by whimbrells. recent findings (J aramillo, unpublished data) Competition is probably an important factor struc- showed a departure from that pattern, suggesting turing the intertidal soft-bottom communities, as that other factors (e.g., seasonality) also affect it has been shown for polychaetes of the northern species richness, abundance and biomass of the hemisphere (e.g., Levin 1981, 1982). macroinfauna. Predation by fish and birds has been suggested as important factors regulating macroinfaunal Subtidal, soft-bottom habitats abundances of the Chilean sandy beach commu- nity (e.g., Jaramillo et al. 1980). Pequefio (1979) In comparison with intertidal habitats, the subtidal showed that Eleginops maclovinus feeds on soft-bottom communities have been less studied. Emerita analoga in sandy beaches of south cen- Most of the research in these systems is descrip- tral Chile. Whimbrels (Numenius phaeopus) and tive and mostly focuses on the following prob- sanderlings (Calidris spp.) have also been ob- lems: (a) physical and chemical factors structur- served consuming Emerita analoga in the swash ing the macroinvertebrate communities (not con- zone of exposed beaches. However, experimental sidering biological processes, or using experi- studies to test the effect of fish and bird predation mental manipulations), (b) biogeochemical pro- on the benthic macroinfauna are not available. cesses occurring in the sediments (especially re- Experimental studies carried out on sandy beach lated to massive prokaryotic sulphur bacterial species of the eastern USA showed that competi- mats such as Thioploca spp.; Fossing et al. 1995), tion is indeed important in amphipod guilds and (c) environmental impact of anthropogenic (Croker & Hatfield 1980). Even when no such activities in the soft-bottom communities. As in experimental studies have been carried out in other systems, the majority of the studies are Chile in sandy beaches, some evidence suggests concentrated on a small fraction of the continen- that such kinds of interactions could be impor- tal shelf (northern Chile: Antofagasta, central tant. For example, the size-structure in Emerita Chile: Valparafso, south central Chile: Concepci6n analoga aggregations in the swash zone of sandy and southern Chile: Punta Arenas) and have been beaches, and the common inverse relationship conducted between 20 and 150 m deep. Thus, between body size and abundance of this crab most of the existing information comes from up- could be due to biological interactions (J aramillo, welling ecosystems, and little is known from the unpublished data). fjords located between Chiloe and Cape Horn. As for sandy beaches, the community structure These are important biases in the quantity and of the intertidal estuarine macroinfauna has been quality of the existing information. In this sec- mainly analyzed in relation to physical factors, tion, we present the most relevant patterns and such as water salinity gradients along estuaries processes in the different soft-bottom benthic and substratum characteristics (Bertnin 1984, systems based on previous studies and reviews 1989, Jaramillo et al. 1985, Donoso 1991, Quij6n (e.g., Arntz et al. 1991, Gallardo et al. 1995). & Jaramillo 1993, 1996, Turner 1984). As it has The farshore soft-bottom subtidal environment been observed in other estuarine temperate areas (ranging from about 30 to 200 m in depth) pre- (e.g., McLusky 1971), the finest and richest sedi- sents two special characteristics strongly associ- ments in organic matter content support the high- ated with (1) upwelled waters (in northern and est abundances and biomasses, while sandy bot- central Chile, Arntz et al. 1991 ), and (2) high toms located closer to estuarine mouths support level of habitat heterogeneity in the south (fjords higher species richness (e.g., Bertnin 1984, and thousands of inner channels; Viviani 1979). Jaramillo et al. 1985). In estuarine areas of south Between Arica and Chiloe, and especially in cen- central Chile epibenthic predation has been ex- tral Chile, the basic taxonomy of dominant groups perimentally studied. Venegas (1992) observed a of macroinvertebrates is generally well known 812 FERNANDEZ ET AL.

(e.g., Annelida (Polychaeta), Wesenberg-Lund The soft-bottom communities of the upwelling 1962, Hartmann-Schroeder 1962, Hartmann- ecosystem (northern and central Chile) have spe- Schroeder & Hartmann 1965, Carrasco 1974, cial characteristics such as the scarcity of large 1976a,b, 1977, Rozbaczylo 1985 and Rozbaczylo macroinfauna (>1.0 mm), high abundance of small & Salgado 1993; Mollusca (Solenogastra, macroinfauna (mainly polychaetes < 1.0 mm), and Caudofoveata, Gastropoda and Bivalvia), Riveros- the presence of massive prokaryotic sulfur bacte- Zufiiga & Reyes 1950, Soot-Ryen 1959, Stuardo rial mats (mainly Thioploca spp., Gallardo 1963, 1960, 1962, Ramorino 1968, Villarroel 1971, 1977a). The presence of large prokaryotic com- Marincovich 1973, Osorio et al. 1979, Osorio munities (Thioploca bottoms) has led to the sug- 1981, Ponder 1983 and De Castellanos 1992; gestion that oxyg~n availability is the major struc- Crustacea (Decapoda), Garth 1957 and Retamal turing factor shaping benthic communities in this 1981; Echinodermata (Ophiuroidea), Castillo area (Gallardo 1963, 1968, 1977a, b, 1985, 1968 and Larrafn 1995). There are some groups of Hartmann-Schroeder & Hartmann 1965, Carrasco invertebrates whose taxonomic identification is &Gallardo 1983,Arntzetal.1985, 199l,Carrasco particularly difficult and needs revision, such as et al. 1988, Gallardo et al. 1995). In general, and Anthozoa, Nemertini, Nematoda, Oligochaeta, from a taxonomic point of view, the macrofauna Pycnogonida, Cephalocarida, Cumacea, of central and northern Chile and the Peruvian Amphipoda, Isopoda and Ostracoda. A recent shelves are very similar (Arntz et al. 1991 ). How- taxonomic monograph about Chilean ever, the abundance of macrofauna off Peru is Protobranchia bivalves (as Nucula, Ennucula, lower than in central Chile by at least one order of Propeleda, Tindariposis, Silicula, Yoldia, magnitude (see Rowe 1971 and Arntz et al. 1991). Yoldiella, Malletia, Tindaria and Acharax) has The central Chile shelf seems to be a more favor- helped clarify the status of deposit-feeder bivalves able habitat for benthic colonization of along the Chilean coast (Villarroel & Stuardo macroinfauna because of the higher input of oxy- 1999). No equivalent work exists for the inverte- gen to the benthos during the autumn and winter brates of the meiofauna (e.g., Nematoda, seasons (Ahumada et al. 1983, Ahumada et al. Copepoda, Foraminifera) and microfauna (e.g., 1991, Gallardo et al. 1995). In fact, the oxygen- Ciliophora, Amoebida). More intensive samplings ated waters affecJ positively the diversity, abun- along the Chilean shelf (especially in the fjords dance and biomass of sublittoral benthos in the area) could bring up new species, although major ·Peruvian continental shelf in inter-year cycles of changes in the total number of species are not the "El Nifio" events (Tarazona 1984 ). The expected. macroinfaunal benthos is clearly dominated in As for most ecological systems, it is difficult to numbers by very small species of Polychaeta determine the exact number of species that coex- (e.g., up to 2·1 03 ind/0.1 m2 and approximately ist in the soft-bottom communities. In general, 80% of the sample, Valdovinos 1998) and con- local communities in northern and central Chile tains very few major taxa such as Crustacea are composed by between 15 and 85 taxa of epi- (mainly Amphipoda), Mollusca (many Bivalvia and infaunal species >1 mm (e.g., Valdovinos and few Gastropoda), and others (e.g., Nemertea 1998). There is no information for small-sized and Cnidaria; Carrasco & Gallardo 1983, species of meiofauna and microfauna that inhabit Valdovinos 1998). Many important groups of within bed matrix of the sediments. In southern macroinfaunal benthos are missing in northern Chile, the number of species is clearly higher. A and central Chile, when compared with the fjords bathymetric trend in species richness of local ecosystem of southern Chile (Gallardo et al. 1995), macrobenthic communities, with maximum val- the tropics or Antarctica (i.e., Gallardo et al. ues in shallow waters, has been reported for north- 1977). ern (J aramillo et al. 1998), central (Gallardo et al. Zonation patterns for the Arauco Gulf (Central 1995), and south central Chile (Valdovinos 1998). Chile) have been extensively described and dis- This negative bathymetric trend in species rich- cussed by Valdovinos (1998, see more details of ness is explained by the effect of anoxic-hypoxic this work below in this paragraph), but other waters in deeper areas (see below). The fjord area Chilean localities are not well known because of of southern Chile shows the opposite trend (Di low spatial resolution in the samples and a poor Geronimo et al. 1991 ), explained by the effect of characterization of the environment (e.g., a strong tidal current and mixohaline waters in granulometry, organic matter, contaminants). The shallow bottoms (Viviani 1979). However, more soft bottoms of the Arauco Gulf exhibit shallow information is necessary to support this general and intermediate depth patches closely associ- trend and the underlying processes. ated with a deeper matrix, forming a complex mosaic in which patch number and configuration, DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 813

connectivity, b9undary shapes, and overall het- Identification of main human impacts affecting erogeneity operate to affect the flows of energy, nearshore ecosystems matter, and species. In this area, the wind plays an important role in accentuating the differences Several types of human impacts clearly affecting that exist between the seascape units. Distur- nearshore ecosystems can be identified along the bance pulses, such as storms and upwellings, coast of Chile, although the intensity, extent, and differentially affect the marine basin depending persistence of these sources vary geographically on the localization of such events. Winter storms (Tables 3 and 4). The predominance of specific affect shallow areas (<15 m), favoring the domi- activities in different regions is clear; mining nance of a reduced number of opportunistic spe- takes place mostly in northern Chile, industries, cies. Longshore currents produce erosion and forestry and agriculture are the main productive movement of the surface sediment, causing mor- activities in Central and Southern Chile, and tality of smaller organisms but not of larger indi- aquaculture peaks in the Austral Region. The viduals that seek shelter deeper in the sediment. most important human impacts along the Chilean The hypoxia-anoxia conditions generated during coast, in terms of geographical extent and persis- the spring-summer upwellings affect specially tence,are sewage discharges and the exploitation organisms residing in deeper zones of the basin of invertebrates and algae in rocky shores (Tables (>40 m) and favor the dominance of a reduced 3 and 4; Gross & Hajek 1998). The V Region has number of opportunistic species with either ( 1) a the largest human population and consequently physiological range wide enough to support oxy- the highest direct and indirect sewage discharges, gen depletion and/or (2) a life cycle synchronized followed by the VIII Region, both in population to such conditions. Diversity of the benthic size and, pollution resulting from human settle- macrofauna, dominated by species with little tol- ment (sewage and industry discharges). Although erance to hypoxia-anoxia, reaches its maximum the effect of sea wage discharges on the structure in zones located at intermediate depths where and functioning of coastal communities is not winter storms and spring-summer upwellings do well known, it is clear that fishing has a strong not have great effects. Abundance, biomass, spe- effect on coastal ecosystems (see above). Areas cies richness, and dominance of guilds are non- with smaller human population sizes on the coast linear functions of the organic matter content of tend to have lower landing of both benthic inver- the sediment in the Arauco Gulf; shallow sandy tebrates and fish, although there is not a direct areas, poor in organic matter, are dominated by relationship between coastal human population suspensivores, while the deposit-feeders domi- size and landings. nate in deeper, muddy sediments rich in organic The existing ecological information indicates matter content. This observation suggests that the that in rocky intertidal and shallow rocky bot- distribution of guilds is fundamentally controlled toms, the most important human impact is the by food availability and by wind-driven perturb- collection of invertebrates and macroalgae by ing agents. It is not known if the pattern of species artisanal fishermen as well as occasional gather- abundance and the dominant factors affecting the ers. Collection of invertebrates and macroalgae macroinfauna in this particular area may also for human consumption can be traced back to occur in other localities. hunter-gatherers (9,000 years ago) in northern Biological processes affecting subtidal soft- and central Chile (Llagostera 1979, Jerardino et bottom communities have not yet been experi- al. 1992). However the introduction of diving mentally quantified. It is possible that, as in many technology and the access to new foreign markets other shelf coasts of the world, top-down factors over the past few decades has produced an expo- play an important role in the regulation of local nential increase in exploitation rates (currently at communities. In the soft-bottom of central Chile, 432,587 annual tons), which has led to symptoms there are few carnivore species that appear to of overexploitation of the main target species. have a much stronger effect than the rest of the Currently more than 22.000 divers and food-gath- carnivores with which they coexist: juveniles of erers are exploiting benthic invertebrates, mostly various species of decapods, such as Cancer on the IV, V, VIII and X Regions (Table 3; coronatus Molina, 1782, C. setosus Molina, 1782 Moreno 2000). A chronic problem in the regula- and C. porteri Rathbun, 1930 (all of them are tion of invertebrate fisheries in Chile is the lack currently exploited), and some predatory poly- of adequate enforcement of fisheries legislation, chaetes errantia of large size, such as Diopatra partly because of the very long coastline and chiliensis, Quatrefages, 1865 and Glycera sparseness of landing sites, but also because of americana Leidy, 1865. the lack of an efficient control of the artisanal fisheries. Another problem is that, despite new TABLE3 00,__. Main human settlements (in cities and over the coast), fisheries landings, aquaculture production, rivers, seawage discharge and pollution in ""' the 12 Administrative Regions of Chile (numbered from north to south). Biogeographic regions and latitudes are also listed

Principales asentamientos humanos (en cuidades y sobre la costa), desembarques, producci6n acufcola, rfos principales, descargas de aguas servidas y contaminaci6n en !as 12 Regiones Administrativas de Chile (de norte a sur). Se indican tambien !as Regiones Biogegnificas y latitudes

Biogeographic Region Latitud Main cities Coastal Main rivers Landings (1997) Number of Aquaculture Direct total Indirect Direct and c Region (South) >I 0.000 people population of main •benthic registered production of seawage sea wage indirect pollution located on (103 hab.) and bfish divers and abenthic and discharge from discharge from the industry the coast resources food bfishes cities located (from rivers, (from rivers, in (*Main ports) (103 ton) gatherers (ton) on the coast J03 m3 aiio) J03 m3 · afio)

18°30' Arica and Iquique* 332 None •8.28 857 all7 23,421 0 8,888 21°30' bJ,373.58 bo II 2J030' • Tocopilla, Antofagasta* 269 Rio Loa •29.90 877 •!84 16,056 4,935 1,872 26°00 and Taltal b331.95 bo "'1 Ill 26°00' Caldera and 31 Rfos Copiap6, •92.82 1076 •6,793 1,486 9,621 14,761 til 29°10' Chafiaral Salado and Huasco b144.80 bo z~ > Rfos Elqui, Limarf 2036 •!0,442 14,562 6,165 z IV 29°10' La Serena and 229 •57.69 8,496 t:l 32°15' Coquimbo* and Choapa b53.80 b41 til N Peruvian or V 32°15' . Quintero, Conc6n, 691 Rios La Ligua, •14.94 922 •133 43,705 558,856 71,806 til Chilean Province W50 Valparaiso*, Vifia del Aconcagua, Marga-marga, b335.28 b315 ..., Mar and San Antonio* Casablanca and Maipo > r-' VI 33°50' All coastalcities (Low) Rios Rape! and •1.16 455 •o (Low) 23,139 47,012 W45' <10.000 Nilahue b0.52 bo VII W45' Constituci6n 30 Rios Mataquito, •!.98 662 •o 1,792 29,195 36°00' Maule and Loanco b3.24 bJ5 VIII 36°00' Talcahuano (San Lota, 499 Rios Itata, •3!.71 3299 •7 ,365 25,333 44,919 176,797 38°30' Vicente)*, Lirquen*, Andalien, Biobio, b3,302.58 b559 Tome, Penco, Lebu and Paicavi Coronel and Arauco IX 38°30' All coastal cities (Low) Rios Imperial •0.32 368 •262 (LOW) 19,697 1,357 39°20' <10.000 and Tolten bO.p5 b5o

Transition zone X 39°20' Puerto Montt*, 166 Rios Calle-Calle, a175.44 8583 •101,569 7,344 14,710 8,814 44°00' Ancud and Castro Bueno and Maullin b23J.97 b2J7,130

Magellanic Province XI 44°00' Aisen 35 Rio Aisen (and many •4.69 2434 •o ? 2,565 607 49°30' more small ones) b45.07 b26,323 XII 49°30' Puerto Natales 135 Many small •42.02 682 ao 8,817 (Low) 64,046 56°00' and Punta Arenas* rivers b5J6 b3,453 DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 815

fisheries legislation (Ley de Pesca y Acuicultura, keyhole limpets of the genus Fissurella (also D.S. N° 430, 1992), there has not been a concomi- heavily collected intertidally and subtidally), c) tant development in the national system of marine kelps of the genus Lessonia (recently collected to protected areas that could serve as a buffer for feed exotic cultivated species such as abalone), d) exploited zones (Hastings & Botsford 1999, the seastar Heliaster helianthus in central Chile Castilla 1999). (massive collections occur in spring and summer On the rocky intertidal shore of central and months), e) beds of Pyura chilensis in subtidal southern Chile, the establishment of two marine areas, which seems to act as engineer species for reserves demonstrated the dramatic effects of the many other invertebrates. We have no ecological subsistence fisheries on the entire intertidal land- information about these beds, which are some- scapes (Moreno et al. 1984, 1986, Castilla & times completely exterminated from large reefs, Duran 1985, Oliva & Castilla 1986). We under- f) beds of mussels, Aulacomya, Chorumytilus and stand much less the ramifications of human ex- others, which provide habitat and recruitment ploitation on rocky subtidal areas, where most of sites for many other species. the artisanal fishing takes place. We do know, The exploitation and use of sandy beaches is however, that many of the species collected have less diverse, and the effect of humans on the the potential to play critical roles in those com- community structure less clear. For example, the munities as predators or structural species. From clam Mesodesma donacium is the only inverte- the wide diversity of species collected by humans brate species widely fished in the surf zone and the ones whose collection has the potentially most shallow subtidal areas of many exposed sandy harmful consequences for the rest of the commu- beaches from Arica to Chiloe Island (Tarifefio nity are: a) the muricid Concholepas concholepas 1980). This resource suffers a persistent human (heavily collected intertidally and subtidally), b) impact that may have affected natural popula-

TABLE4

Main sources of human impact observed in the different administrative Regions of Chile

Principales tipos de impacto humano observado en las diferentes Regiones Administrativas de Chile

Main sources of human impact observed in the Chilean Coast Administrative Regions of Chile I n m N v ~ wvm a x ~ w

Overexploitation of benthic resources Introduced benthic species ol ol ol ,I ,1,2 Pollution by sewage discharges Pollution by the fishing industry (organic discharges) Pollution derived from aquaculture (Pacific salmon): organic matter, antibiotics, antiparasites Chemical pollution from different industries Pollution from mining Pollution due to the use of anti-fouling in harbors and aquaculture Pollution from pest controls (agriculture) Pollution from pest controls (others) Oil spills from ships Oil pollution (oil platforms) Oil pollution (other sources) Dredging of main channels in Chilean Harbors Pollution from polluted rivers (several types) Construction of Port facilities

1Pacific Oyster (in the Chilean coast 3,203 tons are harvested annually) 2Red abalone (in the Chilean coast 1 ton is harvested annually) 816 FERNANDEZ ET AL. tions since landings have decreased dramatically nities are still unknown. The emerging industry in the last 3 years (see Jaramillo et al. 1994). of abalone (and also sea urchin aquaculture) has However, the effectof persistent (or occasional, contributed to the local decimation of the brown see below) removal' of Mesodesma on the sandy algae Lessonia spp. populations. Lessonia spp. is beach community is unknown. used as the main food item for both cultured In contrast to the geographically extensive in- species and its extraction can have severe conse- vertebrate and macroalgal fisheries, other human quences in coastal habitats where these macroalgae activities are concentrated in some regions, among are dominant structural species (see above). Al- them aquaculture, copper and iron mining, dis- though aquaculture of both native and introduced charges of organic matter from the fishing indus- species is currently concentrated in a few regions, try and chemical pollutants from industry and it could extend to the rest of the country in the agriculture (Tables 3 and 4 ). At present, aquacul- near future with the incorporation of new species. ture targets two groups of species in specific Another localized human activity is the copper regions along the coast of Chile: natives and and iron mining that has been taking place for introduced. Among the native ones, Argopecten several decades in northern Chile. For instance, purpuratus constitutes most of the emerging in- in northern Chile (I-III Regions) the average con- dustry taking place in the IV Region, but the centration of copper in sea water and sediments is potential for aquaculture of other native inverte- three times higher than in the rest of the country, brate species is being investigated in Chile (e.g., and well above the international standards clam, limpet, trumulco, sea urchin, Chilean hake). (Hernandez 1998). Other heavy metals, such as Introduced species are also cultured in Chile (e.g., Hg and Pb also show higher concentrations in Pacific salmon), or are planned to be cultured northern Chile, while the concentration of Cad- based on current experimental projects (e.g., Pa- mium in sediments is higher in the XI and XII cific halibut, hiromi, abalone). Probably the most (Hernandez 1998). In all cases strong spatial varia- striking case of aquaculture of introduced species tion in the concentration of heavy metals has been is the Pacific salmon, that fluorished in southern found (Hernandez 1998). In the case of Chile in the last decade (Table 3 and 4) and now Antofagasta Bay, major steps to avoid pollution amounts to 43% of the total income from fish at the MEI production site over the last years have products perceived by the country. Despite the brought levels of copper concentration back to fact that the Fishing and Aquaculture Law explic- normal (Hernandez 1998). Recent studies showed itly indicates that aquaculture activities should that the two most important mining activities in not .affect the ecosystem, little has been done in the country have caused dramatic ecological im- this respect. Furthermore, the introduction of spe- pacts on intertidal and subtidal marine environ- cies for aquaculture was allowed in the new leg- ments; copper tailing produces more ecological islation. The presence of free salmon in the south perturbation than iron (Vasquez et al. 2000). Al- (escaped from pens), the intensive use of antibi- though reports of the effect of pollutants on the otics and other chemicals to control salmon para- macroinfauna in sandy beaches are limited, a sites (but also affecting molting of crustaceans in significant effect of mine tailings on general), and severe eutrophication of the system macroinfaunal density and biomass has also been are among the many impacts of salmon aquacul- shown (Chaiiaral, ea. 26° S; Castilla 1983). Other ture that have not yet been evaluated. Due to studies showed that solid and liquid waste (from escapes of salmon from pens and the ranching mining, but also from human settlements) re- activities since the early SO's, four species of leased into the sea disrupt the distribution and salmon can be found in the north patagonian abundance of brown algae populations (Castilla region of Chile: Salmo salar (Atlantic Salmon), & Nealler 1978, Vasquez & Guerra 1996, Vasquez Oncorhynchus tshawytscha (Chinook), 0. kisuch et al. 1999). (Coho), and 0. mykiss (Rainbow trout). The Chi- Some human activities can have intense impact nook is known to have wild populations in some on the nearshore community only during short rivers and at sea, the Rainbow trout shows wild periods of time, although the actual effect on the populations in almost all the Chilean rivers, and marine community might be long lasting. Among the escaped Coho salmon has established wild them are vacationers, oil spills, dredging, and populations in recent years in the Aysen rivers ballast seawater. Oil spills do have an affect on and fjords (Soto et el. 1997). One of the major macroinfaunal density and biomass in sandy potential disturbances related to these introduc- beaches (ea. 32° S; Castilla et al. 1977), and tions, through direct or indirect effects, is the affect survival of marine birds and mammals. replacement of high trophic-level native preda- Occasional exploitation of sandy beach inverte- tors; the effects on the rest of the natural commu- brates such as M. donacium occurs in summer DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 817

time, by beach visitors. Fishing effort exerted by 2. High cover of Mazzaella laminarioides and beach visitors is comparable to the artisanal fish- Ulva spp. in the midlittoral of protected and ery (De Ruyck & Soares, unpublished data); how- semiprotected rocky shores is found when herbi- ever, experimental studies did not show any sig- vores have been removed by humans (Moreno et nificant effect of human exclusion on al. 1984, Oliva & Castilla 1986). The high cover macroinfaunal abundance in a sandy beach of of these two algal species is a good indicator only south central Chile (Mehuin, ea. 39° S, Jaramillo in extended rocky shore areas, but can not be used et al. 1996). Construction of new roads that al- in the limits between rocky and sandy beaches lows easy access to coastal areas may increase the where the same effect is apparently produced by number of visitors to the intertidal zone and their sand abrasion. impact on these ecosystems. To date, human im- 3. Large plants of Durvillaea antarctica are pact is low in some areas such as in intertidal present only in the very low intertidal or shallow estuarine flats of south central Chile. However, in subtidal rocks of exposed fronts, less accessible some of these estuaries, large domestic verte- to humans, and absent from protected and semi brates such as cows and pigs from nearby farming protected benches where humans exploitation is communities produce occasional, but large me- high (Castilla & Bustamante 1989, Bustamante & chanical disturbances, although the actual effect Castilla 1990). has not been quantified. Similarly, mechanical These are the most easily perceived effects of disturbance by fishing boats on the mud flats is humans in rocky intertidal communities along unknown. central and southern Chile. The distribution of So far there are no written reports of marine intertidal species and the environmental condi- invertebrate or fish species introduced to Chile tions in northern Chile and the fjord region differ (other than related to aquaculture activities).lt is from the systems where experimental human ex- possible that the circulation pattern along the clusion studies were conducted. Thus, the indica- coast of Chile does not favour successful coloni- tors proposed above can only be of use between zation of exotic species, but with increasing fre- 33 and 41 °S. Indicators of human use for the rest quency of international trade the potential for of the country are also needed, especially for species introduction increases. Although there northern Chile where exploitation of intertidal are regulations for ballast seawater, enforcement communities is more pronounced (Table 3). is not always achieved and a variety of species Other indicators of human impact (specifically could be introduced, especially in major ports and of iron and copper mining and of sewage dis- bays. The European heron (Cornelius, Marquet & charges) are the presence and abundance of Navarrete, unpublished data) is probably one of Lessonia trabeculata (subtidal) and L. nigrescens the examples of introduced species that is defi- (intertidal) and the community associated with nitely using the intertidal zone, although its im- their holdfasts. Tailing from copper mining ap- pact on the benthic community is still unknown. pears to cause more ecological perturbations than The use of indicators to assess the actual impact that from Fe mining in northern Chile (V asquez et of the different human activities on nearshore al. 1999). In severe cases of contamination (e.g., communities is desirable, but difficult to achieve. 2 km from copper mining effluents), the Although some variables of human impact can be macroalgae themselves may disappear or be found easily quantified (e.g., copper levels, or Escheri­ in bad condition, with no macroinvertebrates spe- chia coli), the actual impact on the system is not cies inside or nearby the holdfasts (V asquez et al. easy to assess. However, the current knowledge 1999). Similar ecological damages have been of the rocky intertidal system and the main fac- documented for rocky and sandy intertidal com- tors structuring the community between 33 and munities in northern Chile (El Salvador, Castilla 41 o S provided the grounds for developing indi- & Nealler 1978). At lower pollution levels, cators of severe human exploitation (Moreno, Lessonia survival increases, and the holdfast com- unpublished data). Among others, the following munity (diversity of species in the holdfast-mi- indicators of severe human exploitation were rec- crocosm) provides a sensitive method to assess ognized: copper contamination (Vasquez & Vega unpub- 1. Size distributions of edible invertebrates are lished data). If proven efficient for other lati- truncated in the larger size classes (mainly for tudes, this indicator could be used to assess hu- Fissurella spp. and Concholepas concholepas) in man impact in other regions of Chile. Another all types of intertidal habitats impacted by hu- indicator of pollution is the extensive dominance mans (Moreno et al. 1984, Oliva & Castilla 1986, in the entire intertidal zone by the green alga Castilla & Dunin 1985, Moreno et al. 1986, Dunin Enteromorpha in polluted areas. Enteromorpha & Castilla 1989). compresa from Caleta Palito, one of the highest 818 FERNANDEZ ET AL. copper-enriched coastal localities in northern of potential sites for sitting MP As and the total Chile, tolerates high copper concentration consti- area to be protected are critical. tuting the only species of algae in areas with There is little empirical evidence to suggest mining discharge influence (Correa et al 1996). how much should be conserved in the marine system. The Wold Conservation Union (IUCN) has proposed a goal of20% of the world's coast- INTRUMENTS, NEEDS AND GUIDELINES FOR MARINE line (IUCN 1992), but it is no clear what is the CONSERVATION foundation behind this figure. Other authors have suggested different target areas for protection, Although the establishment of marine conserva- ranging from 10% of the total range of a popula- tion policies takes into consideration scientific, tion (based on the fishery principle of protecting social, economic, and legal criteria, we think that a fraction of the spawning biomass) to 40% of the biological and ecological principles should guide spawning stock for species particularly vulner- the identification of priority geographic regions able to fisheries (Mace 1994 ). Recently Lauck et for conservation. We do not claim that the other al. (1998) suggested that reserves covering about criteria are not important, simply that they should 30% of the fishing grounds are needed to main- play a critical role only after the questions of tain stocks at target levels, considering interme- what needs to be conserved and where to concen- diate levels of uncertainty in the system. These trate conservation efforts have been addressed figures come from MPAs designed mostly for based on biological considerations. From this fisheries purposes. However, it is clear that much perspective, we present and discuss in this sec- of these estimations do not have scientific basis, tion the ( 1) main instruments for marine conser- and there is little agreement on how much should vation used worldwide, (2) basic needs for marine be protected. conservation in Chile, and (3) guidelines forma- Regarding site selection, the best documented rine conservation based on the current knowledge process in the marine system involves the appli- about the ecology and biogeography of the cation of ecological criteria, and for this purpose nearshore ecosystem in Chile. several types of ranking schemes have been used (Kelleher & Kenchington 1992, Odendaal et al. 1995, Salm & Price 1995). These rankings in- Instruments for Marine Conservation clude criteria such as diversity, productivity, representativity of the biogeographic regions, sta- The current crisis of the marine environment (loss tus of the species and habitat, extent of human of biodiversity, habitat alteration, extensive de- use, etc. Hockey & Branch (1997) suggested to clines in population sizes, pollution) was partly consider the middle/edge system in selecting sites contained several decades ago in terrestrial sys- for MP As. While areas of higher diversity are at tems by the designation of national parks and the edge, placing a MP A in the middle of a bio- reserves which protect biotic and abiotic re- geographic region would have positive effects, sources. In the marine environment the use of since higher abundance and reproductive suc.cess protected areas (MPA) is relatively new, but the should be expected in the center of species ranges. number of MPAs worldwide is increasing dra- Furthermore, negative effects, due to variations matically. MP As are being used to protect endan- in the ranges of distribution caused by climate gered species and critical life history stages, main- changes, would be avoided. Within a biogeo- tain biodiversity, spawning biomass of exploited graphic region, a range of habitat types (e.g., species, and intra-specific genetic diversity, pro- sandy beaches, rocky shores, estuaries, different tect specific habitats, improve yield, and also for conditions of wave exposure, etc.) and especially educational purposes. However, the sudden inter- vulnerable habitats need to be incorporated est in the creation ofMPAs is driven more by the (Hockey & Branch 1997). Ballantine (1997) dis- collapse of fisheries than by the state of cussed not only the criterium of representati vine ss biodiversity. Nevertheless, major efforts have also but also the replication and connectivity among been directed to the creation of MP As as reser- MPAs. It is also important to consider whether voirs of biodi versity ,. and currently MAPs are the the area includes exploited species and its "per- main instruments for marine conservation. We meability" to adjacent areas. Finally, the condi- think that, as in terrestrial systems, the major goal tions of the selected area are not trivial; a pristine of MP As should be the protection of biodiversity area, or at least one that is not heavily impacted, (e.g., species and habitat diversity, ecological is preferable. After biological criteria have been processes). From this perspective, the selection applied, general consideration about the feasibil- ity of placing a marine reserve within the range of DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 819 areas of interest needs to be evaluated (i.e., exter- objectives as well as management and conserva- nal threats, conflicts of interest, costs of estab- tion actions (Morales & Ponce 1997). According lishing and maintaining a MPA). For instance, to Morales & Ponce ( 1997), the legal framework management and enforcement of marine reserves for the implementation of marine protected areas is established adjacent to terrestrial reserves may be substantial; however, the mechanisms for the imple- more easily achieved (Attwood et al. 1997, Hockey mentation need yet to be developed. As yet, most & Branch 1997). The additional benefit of having efforts have been directed toward the creation of a MPA adjacent to terrestrial reserves is the eradi- partially protected areas for fisheries purposes (Man- cation of problems related to land use. Efforts agement and Exploitation Areas, MEA), one Ma- also need to be made to consider regional and rine Reserve (as a genetic reserve of the overex- international regulations. ploited Northern scallop Argopecten purpuratus; Besides the considerations of the total area to Morales & Ponce 1997) and only recently three be protected and the target regions for MP As, the submarine parks have been created at Eastern Island design of the network is also of great importance. by the Subsecretaria de Marina. Legally these pro- The factors contributing to the success or failure tected areas are not Marine Parks (but Coastal and of MPAs are difficult to decipher, and very often Marine Protected Areas, because only the Fisheries the failure has been attributed to inadequate man- Administration has the mechanisms to create Ma- agement or enforcement. However, the design is rine Parks). In addition, there are other types of also likely to affect the success of the MPA. A protected areas (marine concessions; Castilla 1986, number of concepts, which are being applied to 1996). Considering the basic information needed MPAs in terrestrial systems, deserve attention; for site selection, designation of total area to be the SLOSS debate (Simberloff 1988) and the con- protected, and the design of the interconnected net- nectivity between MP As are at the center of the work, in the next two sections we discuss the basic discussion on reserve design. As yet, the di- needs to implement such a MPA network in Chile, chotomy in the design ofMPAs (e.g., size) stems and propose some guidelines. from the intended purpose, although this situa- tion may change as more evidence becomes avail- able. The debate concerning the edge effects has Basic Needs consequences on the transfer of propagules (or other life history stages), and also pollutants, In this section we will outline the basic needs for across reserve boundaries. This issue is probably marine conservation plans in Chile derived from of greatest importance for fisheries reserves, our overview. However, we recognize that there where spillover to fishing areas needs to be as- are other needs in the legal system and social sured (Attwood et al. 1997). However, spacing aspects that need to be considered, and those we and reserve size is also of major importance for will briefly discuss. The following are among the MPAs created as reservoirs of biodiversity, al- biological and ecological needs we identified: though until now contradictory results have been 1. Some gaps in information regarding the tax- found (McNeil & Fairweather 1993). The reality onomy and large-scale patterns of species distribu- is that little can be said regarding optimum MPA tion, for some taxonomic groups. We think that more network design based on scientific evidence, and taxonomic and molecular work may help clarify the the experience gained from a MP A network may status of some species and also show the existence of not necessarily be effective in other geographic new species. However, since no large variations in areas since the design is strongly dictated by the the total number of species are expected, the current biology of the species or communities that need large-scale patterns of species distribution may not to be protected, and the local oceanographic con- substantially change in the future. ditions (Nowlis & Roberts 1997). 2. An urgent need of studies addressing the The instruments related to the protection of causal factors generating the patterns of species aquatic areas have existed in Chile since 1960. distribution observed, especially in southern The concept of marine protected area, and the Chile. This information is needed for all taxo- need to establish them, is present in eight Chilean nomic groups, since different diversity patterns laws and four decrees. In addition, Chile is party are observed for different taxa. to a number of international conventions which 3. A need to organize the existing biological promote the creation of MP As for different pur- and ecological information using some criteria poses. Three categories of protection are recog- (e.g., larval ecology). This work would require nized: (1) areas for management and exploitation the join efforts of a team of recognized marine of benthic resources, (2) marine reserves, and (3) scientists from Chile, but unfortunately, this type marine parks. Each of these have a different set of of project is not a strong candidate for funding in 820 FERNANDEZ ET AL. the Chilean research funding system. Along the spills, and other environmental factors. Insurance same line, a team of recognized scientists could factors have been proposed as a way to qualita- play a critical role in determining the criteria for tively assign these risks. Records on most of these site selection, evaluation, and management of factors have not yet been compiled, and in many MPAs. This strategy was used in South Africa, cases, the information is widespread or not avail- where the task group reviewed not only the status able in Chile. For instance, the effect of fishing of marine conservation and evaluated existing on the whole ecosystem (e.g., removal of large or marine reserves, but also proposed action plans. key predators, bycatch) or habitat fragmentation 4. A need to classify the conservation status of (e.g., benthic fisheries) has not yet been evalu- species and identify particular groups of species ated. that need to be considered separately in a network 11. A need to evaluate the effect of species of marine protected areas. For instance, data on introduced for aquaculture purposes on local minimum viable population size are available only biodiversity and ecosystem functioning (local, for 15 of the I 01 exploited marine species in Chile but also potential for dispersal). This imposes a (Moreno 2000). For most exploited species stock major constraint on the success of MP As as reser- assessments are not regularly conducted, and in- voirs of biodiversity (e.g, salmonids in Southern formation on genetic diversity is non-existing. Chile). 5. A deficiency in information about life his- 12. A need to analyze, adopt/modify/extend to tory of most species. Modes of development (rang- local conditions (ecological, social) the criteria ing from direct development to long planktonic proposed for site selection (e.g., Salm & Price life) affect the replenishment patterns of marine 1995). populations, and this single factor could greatly In addition, we recognize other needs that may affect the design and effectiveness of MPAs. have an effect on any marine conservation strat- 6. A necessity in information about coastal egy in Chile. It is a priority to quickly establish an currents in order to better understand possible efficient system for the implementation, manage- ways of larval transport in the nearshore, and its ment and enforcement of MPAs. It is also a prior- effect on population and community dynamics. ity to provide the national agency interested in As yet, most oceanographic studies have been marine conservation the tools to create MP As as conducted on the continental shelf, and little has reservoirs ofbiodiversity (e.g., CONAMA), rather been done in coastal waters. than relying on, agencies interested in MP As only 7. A need for more information about commu- for management purposes. Additional research nity structure and ecosystem functioning, espe- fundings (e.g., sectorial programs) may have an cially highlighting the effect of human impact; enormous impact on the quality and amount of currently this information comes only from very information that can be obtained in relatively few geographic regions. More information about short time. It may also help to achieve a higher community structure for other areas of the coast level of involvement of scientists in conserva- is needed, particularly considering the strong dif- tion, including outreach programs. Educational ferences in temperature, circulation patterns, habi- programs directed to conservation in general, and tat heterogeneity, species composition, as well as especially to marine conservation, need to be the effect of upwelling and El Nifio along the implemented in Chile. We think that social pres- 4000 km of coastline. Experimental work has sure for more immediate conservation measures been mostly conducted on rocky intertidal shores, may result through educational programs. Finally, and more information about other types of sys- we think that the bureaucratic system in Chile tems is needed (e.g., soft-bottoms). does not favor the possibility of debate about 8. A need for more studies to assess the actual conservation issues. For instance, the general effect of upwellings on coastal community dy- public does not have easy access to public infor- namics; upwellings are a major oceanographic mation (e.g., stock assessment of exploited spe- component of the Chilean ecosystem. cies). Access to such information is important 9. That indicators of human impact need to be because conservation groups could do indepen- developed for more systems and expanded for dent analysis, and generate informative/educa- rocky shores to northern and southern Chile. The tive debates. indicators currently available are based on stud- ies conducted in a few geographic regions, and it is unclear whether those indicators can be used in Guidelines for Marine Conservation in Chile other areas of the country. 10. The need to evaluate the frequency, extent Since the dispersed efforts to create a network of and effects of pollution, fisheries, storms, oil MPAs in Chile have not yet yielded results, we DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 821 think that future plans could be benefited from ing coastal National Parks. Actually, many sites the incorporation of the experience gained in identified for the conservation of the biodiversity other geographic areas of the world. For instance, in Chile (terrestrial flora and fauna; Mufioz et al. major efforts in defining priority areas for con- 1996) could be extended to intertidal or shallow servation in Chile need to be taken, rather than subtidal areas, since they are located on the coast following the alternative, opportunistic approach and cover both biogeographic regions. We think of sitting MP As in the less conflicting sites or that Ormaziibal' s proposal ( 1993) is a plausible sites not yet occupied by MEAs or assigned for step that does not necessarily exclude a future aquaculture purposes. For instance, the spatial marine conservation plan with specific objec- arrangement of the more than 220 MEAs requested tives. In fact, there are already 11 protected areas so far (Dario Rivas, pers. comm.) responds to the in the National System of protected areas (Na- opportunistic requirement of fishermen unions, tional Park, National Reserve, or National Monu- and does not respond to a coordinated plan of the ment) that include a section of sea bottom (Table fisheries' administration to allow for interspaced 5) and 10 more that are adjacent to the coast, or no-take zones. In fact, the wide spread of MEAs include coastal areas, extendeding along the coast along the coast of Chile poses serious problems to of Chile. However, we agree with Castilla (1996) the potential sitting of MP As since in some re- that the design of a marine reserve network can- gions (e.g., IV and V) virtually the whole coast not be completely accommodated to terrestrial has already been assigned to MEAs. We think that conservation plans and needs to take into account MEAs are an excellent management strategy for the latitudinal variation in species diversity and benthic resources, and they could complement ecosystem processes (Castilla 1996). In addition, any conservation plan, but caution should be ex- the size of the resulting MP As, the orientation, erted to balance the possible "competition" for and the spacing between them may not allow suitable sites between MPAs for conservation exchange of propagules or adult stages. and management purposes. As it has been proposed for Chile (Castilla The need to preserve species and ecological 1996) and for other areas (e.g., South Africa, processes along the Chilean coast has already Hockey & Branch 1994, Hockey & Branch 1997), been discussed (e.g., Castilla 1976, 1986; we think that a MPA network needs to be de- Ormaziibal 1993), and potential sites have even signed in such a way that (1) biogeographic re- been suggested. Ormaziibal (1993) suggested to gions are well represented (including Oceanic incorporate the littoral zone adjacent to the exist- Islands), (2) unique or special oceanographic sys-

TABLE 5

Units of the National System of Protected Areas that include a section of the sea bottom, and of the National System of Wild Protected Areas of Chile (SNAPE) adjacent to the coast or that include coastal area. NM indicates National Monument, NR National Reserve, and NP National Park

Unidad del Sistema Nacional de Areas Protegidas que incluye una secci6n de fondo marina y del Sistema Nacional de Areas Silvestres Protegidas adyacentes a la costa, o que incluyen una secci6n de area costera. NM indica Monumento Nacional, NR Reserva Nacional y NP Parque Nacional

Units of the National System of Protected Units of the National System of Wild Areas that include sections of sea bottom Protected Areas of Chile (SNAPE) adjacent to the coast or that include coastal areas

Isla Magdalena (NP) Pan de Azucar (NP) Laguna San Rafael (NP) Llanos de Chile (NP) Bernado O'Higgins (NP) Bosque Fray Jorge(NP) Alberto M. de Agostini (NP) Archipielago Juan Fernandez (NP) Cabo de Hornos (NP) Rapa Nui (NP, already established) Las Guaitecas (NR) Chiloe (NP) Katalalixar (NR) Isla Gamblin (NP) Alacalufes (NR) Pinguino de Humboldt (NR) La Portada (NM) Laguna Torca (NR) Cinco Hermanas (NM) Isla Cachagua (NM) Los Pingiiinos (NM) 822 FERNANDEZ ET AL. terns within a biogeographic region are protected, (Santelices 1980, Camus 1998, Brazeiro 1999, and (3) all habitats are well represented (this Navarrete & Ferniindez, unpublished data). North includes different habitat types as well as wave of about 30 os there is also a discontinuity in the exposures). Additional priority areas may need to diversity of native species of birds, mammals, be established to protect endangered species. and reptiles associated to littoral environments, Based on our overview and ongoing studies,· we and endemicity peaks. Within the Humboldt re- think that the two biogeographic regions identi- gion, the effect of upwellings and El Nifio event fied by most authors need to be represented in a as large-scale oceanographic processes need to be network of MPAs in Chile. Diversity is definitely considered. A good representativity of habitat higher south of 40-45 os (although not for all types in each MP A is desirable. taxonomic groups), but high spots of diversity Castilla (1996) emphasized that MP As should should not be the only issue in site selection in also meet educational purposes. We also believe this case because species composition changes that education is very important, but to meet this dramatically north and south of this latitude. The goal small MPAs could be used and site selection decision of establishing a MPA in Chiloe Island is of large MP As do not need to take into consider- important because of the high diversity of this ation the vicinity of major population settlements area, but it should be kept in mind that this area and educational centers. In our opinion, near- represents the edge of the distribution of most pristine sites should be preferably selected to species. Therefore, at least one large (although avoid highly deteriorated habitats due to anthropic replication within a region is desirable) MPA influence. Marine concessions managed by Chil- needs to be placed south of 45 °S, which should ean Universities could serve for educational pur- include fjords and channels, as well as protected poses, through some incentives. There are cur- and exposed coasts. Special attention to the po- rently five Marine Concessions assigned each to tential impact of salmon aquaculture and escap- the University of Arturo Prat (Huiquique; I ees on no-take zones needs to be taken. Prelimi- Region), Universidad Cat6lica del Norte (La nary modeling results suggest that optimum spac- Herradura, IV Region), U niversidad de Valparafso ing of MP As depends on the dispersal ability of (Montemar, V Region), Pontificia Universidad the target species (Tuck & Possingham 2000). Catolica de Chile (Las Cruces, V Region) and Ongoing studies also suggest that several small U ni versidad de Concepci6n (Dichato, VIII reserves seem to work better for species with long Region). The actual goal and current state of planktonic life, while large reserves seem to be these Marine Concessions is unclear in most cases preferable for species with direct development (except for the reserve of Las Cruces), however (Hastings & Botsford, unpublished data). The the situation could change if special incentives Humboldt Region presents a simplified situation are offered to maintain these areas as pristine in from this perspective because species with plank- exchange for educational services. Other coastal tonic larvae are predominant, and because at any universities may also be considered for this plan. given latitude the mean range size of species does There are no doubts about the deterioration of not change, regardless of modes of development the coastal and the nearshore ecosystems in Chile. (Fermindez, unpublished data). The Magellan area Despite that the economy of the country depends presents the most difficult scenario for the design enormously on the sea, conservation actions have of MP As to assure connectivity, because it com- not yet been a priority in Chile. As yet, all the bines about the same proportion of species with efforts have been directed to obtain the best, short direct development, planktotrophic, and term benefit from the ocean; for instance frac- lecitotrophic larvae, and the range sizes vary on tions of the high economic returns of some activi- average between 10 and 40 degrees (Ferniindez, ties (e.g., salmon aquaculture, sea urchin fishery) unpublished data; range sizes in the sea seem to have not been used to evaluate their impact on the be related to the potential for dispersal of larval marine ecosystem, and to compensate/mitigate stages). Although diversity does not change for for those actions. Only recently the last of the most known taxa within the Humboldt Region, four priorities of the Fisheries Administration, we think that two groups of large MPAs (reser- set conservation plans, started to receive atten- voirs of diversity and ecological processes) should tion although currently most efforts come from be considered, one in the northern region (north the CONAMA. This overview shows that there is of 30 °S) and one south of 30 °S. Several authors substantial (although not complete) knowledge have consistently suggested a small discontinuity about the nearshore ecosystem, and this informa- in species richness, recruitment of intertidal spe- tion could be used to design a conservation plan, cies, and also in B diversity in intertidal rocky and if Chile is going to use the instruments available sandy beach communities at about 30° S in its legal system and meet its international corn- DIVERSITY, DYNAMICS AND BIOGEOGRAPHY OF BENTHIC ECOSYSTEMS IN CHILE 823 promises promoting the creation of MP As as res- ARNTZ WE, 1 TARAZONA, VA GALLARDO, LA ervoirs of bibdiversity in the near future. FLORES, & H SALZWEDEL (1991) Benthic commu- nities in oxygen defficient shelf and upper slope areas of the Pervian and Chilean coast, and changes caused by El Nifio. In: Tyson RV & TH Pearson (eds) Modern ACKNOWLEDGEMENTS and ancient continental shelf anoxia Vol. 58: 131-154. Geological Society Special Publication Edition. This paper is dedicated to the memory of Dr. ATTWOOD CG, JM HARRIS & AJ WILLIAMS (1997) Patricio Sanchez, a pioneer and forerunner in International experience of marine protected areas marine studies in Chile. This work was fully and their relevance to South Africa. South African funded by the FONDAP in Oceanograffa y Journal of Marine Science 18: 311-332. Biologfa Marina, Programa # 3 in Ecologfa y BALLANTINE WJ (1997) Design principles for systems Conservaci6n Marina. We thank Juan Carlos of «no-take>> marine reserves. Fisheries Centre, Uni- versity of British Columbia, Vancouver. 18 pp. Castilla, Sandra Miethke and two anonymous re- BARNES RSK & RN HUGHES (1999) An introduction to viewers for their helpful comments, and Andrea marine ecology. Third Edition. Blackwell Science, Angel, Marcelo Rivadeneira and Alvaro London. 286 pp. Sotomayor for their help. BERLOW EL, SA NA VARRETE, C BRIGGS, BA MENGE & M POWERS ( 1999) Quantifying variation in strengths of species interactions. 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Associated Editor P. Camus Received December 17, 1999; accepted September 21, 2000