PATTERNS of PREY BIOMASS CONSUMPTION by SMALL ODONTOCETES in the NORTHEASTERN COAST of VENEZUELA Lenin E

PATTERNS OF PREY BIOMASS CONSUMPTION BY SMALL ODONTOCETES IN THE NORTHEASTERN COAST OF VENEZUELA Lenin E. Oviedo Correa1,2

ABSTRACT Trophic relationships are conditioned by population dynamics of interacting species in the community (species present, food web connections among them, and the strength of interactions), and on the consequences of these species interactions depend various ecosystem processes such as productivity and nutrient flux. Odontocetes target a wide range of prey items and are adapted to feeding at different depths. The aim of this report is to describe the patterns of prey consumption by small odontocetes, incorporating natural predatory patterns into a potential management scheme of strategic food sources, for both human and marine predators. Using the geo-statistical analysis tool of ArcGIS 9.2, maps illustrating the intensity and location of prey consumption were made for species with a sighting index (SPUE) > 0.15. The biomass consumption emphasized the differences in habitat use by species. The trends in distribution of prey biomass removal by odontocetes particularly suggest a stratification of prey consumption primarily in shelf waters, with a prey biomass that is comprised basically by demersal fish and small pelagics (includingSardinella aurita), and into transition-oceanic depths where most of the predatory pattern would potentially rely on pelagic - mesopelagic squid and myctophids. Overall the spatial tendencies in regionalization presented in this contribution will serve as a base-line to assess ecosystem health and evaluate management scenarios.

Keywords: Atlantic ocean; distribution; food/prey; ecosystem; habitat.

RESUMEN Las relaciones tróficas son reguladas por la dinámica poblacional de las especies que interactúan dentro de la comunidad (especies presentes, conexiones interespecíficas, y nivel de interacción) y de las consecuencias de esas interacciones para procesos del ecosistema como la productividad y el flujo de nutrientes. El objetivo de este reporte es evaluar el patrón de consumo de biomasa por odontocetos de menor tamaño en la costa Nororiental de Venezuela, incorporando patrones de depredación natural a un esquema potencial de manejo de un recurso alimentario estratégico. Por medio de la herramienta de análisis geoestadístico del software ArcGIS 9.2, se elaboraron mapas de densidad en consumo de biomasa de presas para las especies con un índice de avistamiento (SPUE) > 0.15. El consumo de biomasa de presas enfatiza en el uso diferencial de hábitat por especie. La tendencia en la distribución de la remoción de biomasa de presas por cetáceos odontocetos principalmente sugiere la estratificación del habitat, primeramente en el ámbito de la plataforma continental, con un biomasa de presas que estaría constituida por peces demersales y pequeños pelágicos (entre estos S. aurita). Así como en profundidades Transicionales - Oceánicas, donde la mayoría de los patrones de depre- dación dependerían de organismos pelágicos - mesopelágicos, como calamares y peces mictófidos. Las tendencias espaciales en regionalización, como las que se presentan en es reporte, representan una línea base clave para evaluar la salud de los ecosistemas y escenarios de manejo.

Palabras claves: Océano Atlántico, distribución; alimento/presas; ecosistema, hábitat.

1 Proyecto Golfo de la Ballena, Biotropica, Caracas Venezuela. 2 Proyecto Delphinus, Isla de Margarita, [email protected].

Recibido 04-V-2009 Aceptado 13-X-2009

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INTRODUCTION deeper water is likely to offer more niches to be exploited by marine The understanding of food webs life (Heithaus & Dill, 2002; Würsig, entail a detailed perception of factors 2002). Therefore, the complexity in the interface of community and of the cetacean habitat is a key ele- ecosystem ecology. Trophic rela- ment with implications for foraging tionships are conditioned by popula- success, for instance steep sea floor tion dynamics of interacting species slopes, such as those typically asso- in the community (species present, ciated with continental shelf-breaks web connections among them, and provides upwelling opportunities by the strength of interactions) and on forcing nutrient-rich deep-water cur- the consequences of these species in- rents to the surface, thus promoting teractions depend various ecosystem a potentially rich foraging environ- processes such as productivity and ment (Hui, 1979, 1985). This report nutrient flux (Begon et al. 2006). describes the patterns of spatial dis- According to Perez & McAlister tribution in biomass consumption by (1993), fish stocks and marine mam- small odontocete cetaceans within mals are recognized as interacting the marine ecosystems off the north- components of the marine ecosys- eastern coast of Venezuela. This is a tem. For the commercially valuable key area in terms of biodiversity in species, knowledge about the degree the Greater Caribbean eco-region, of competition between fisheries prey abundance is characterized by and marine mammal predators is of the local occurrence of small pelag- vital importance. Cetacean distribu- ic species such as round sardinella tion is generally related to the pres- (Sardinella aurita), associated with ence/absence of their prey (Forcada, habitat productivity due to wind-in- 2002). Due to their relatively high duced upwelling. There has been a energy requirements, cetaceans oc- documented decrease in wind force cur primarily in locations with high since 2004, resulting in weak up- potential prey abundance (Pusineri welling. Consequently, the sardine et al. 2008; Costa, 2002). Odonto- fishery has decreased since 2003, cetes target a wide range of prey reaching a critical point in 2005. items, they can be distributed over Prey depletion has been an in- wide ranges, and change their distri- fluential factor for cetacean popula- bution seasonally, influenced by the tion decrease (particularly common availability of their prey (Forcada, dolphins) in other locations such as 2002). Different species are adapted the Mediterranean basin (Bearzi et to feeding at different depths (Caña- al. 2008), identifying degradation das et al. 2002; Weir et al. 2001; Da- of the food web, where the exploi- vis et al. 1998), base on the fact that tation of marine resources could

246 Rev. Mar. y Cost. ISSN 1659-455X. Vol. 1. 245-257, Diciembre 2009. Patterns of prey biomass consumption by small odontocetes in the northeastern coast of Venezuela lead to additional species loss (Coll sections are comprised by approxi- et al. 2008). The aim of this report mately 37% (>5700 km2) shelf habi- is to describe the patterns of prey tat and 63% (>10500 km2) oceanic consumption by small odontocetes environment off the shelf break: in the study area using a spatial approach, looking at the incorpora- a) The shelf break on the north coast tion natural predatory patterns into of Margarita Island and La Blan- a potential management scheme of quilla Island (approximate area a strategic food source for human 6752 km2): This portion is a tran- and marine predators. sition zone between the neritic and pelagic habitats. Lesser upwelling MATERIALS AND METHODS centers are present in the northern coast of Margarita Island, inclu- Study area ding Macanao Peninsula. Although fishermen use the area, it has the The study area has been subdi- lowest level of disturbance due to vided into four large-scale sections anthropogenic activities. It is quite of the five subdivisions proposed by important to point out that this loca- Acevedo et al. (2007) as important tion is currently considered for oil areas of conservation for misticete industry exploration and develop- cetaceans (Figure 1). Overall the four ment activities in the near future. Figure 1

Study Area in Northeastern Venezuela, divided according to Acevedo et al. (2007): (A) The shelf edge on the north coast of Margarita Island and La Blanquilla Island, (B) Margarita Island’s eastern coast and Margarita-Los Testigos submarine platform, (C) The northern coast of Araya Peninsula, including Margarita, Coche and Cubagua islands, (D) The Cariaco Basin, southwest of Margarita and Cumaná, including the Cariaco Gulf.

Rev. Mar. y Cost. ISSN 1659-455X. Vol. 1. 245-257, Diciembre 2009. 247 Lenin E, Oviedo Correa b) Margarita Island’s eastern coast Park (NP), the human impact on and Margarita-Los Testigos sub- the marine portion of the ecosys- marine platform (approximate area tem is intense. The threats include 3898 km2): The continental shelf fisheries, chemical and acoustic here is wide and relatively even, pollution, development of oil and with both muddy and muddy-sandy gas production facilities, and com- bottom. The latter features mostly mercial shipping traffic. constitute a key shallow neritic habitat, also influenced by the upwe- Small Odontocetes’ Sightings and lling off Carupano’s coast (central Data Analysis Paria Peninsula). This zone is sub- ject to traditional uses of its marine Non systematic and systematic resources by people. Coastal popu- data collection on cetacean encoun- lation densities have been increa- ters (sightings) off northeastern Ven- sing in recent years and there are ezuela have been carried out since also significant land-based sources 1997, resulting in a database with of pollution associated with port records for more than 10 species: development and tourism. Megaptera novaeangliae, Balae- c) The northern coast of Araya Penin- noptera edeni, B. physalus, Physeter sula, including Margarita, Coche macrocephalus, Tursiops truncatus, and Cubagua islands (approxima- Stenella coeruleoalba, S. frontalis, S. te area 1812 km2): This region has attenuata, Grampus griseus, Sotalia complex submarine topography guianensis and Delphinus spp. due to the presence of Margarita, Ninety six sightings records on Coche and Cubagua islands. An five species (Table 1) of small odon- area of upwelling is located off tocetes from 1997-2008 were select- north Araya Peninsula; intensity of ed. All records were analyzed using upwelling is highly influenced by descriptive statistic and integrated the seasonal variations associated into a Geographical Information Sys- to the trade winds annual cycle. tem (ArcGIS 9.2). Observations yield The most important anthropoge- information on date, time, group size, nic impacts here are fisheries, che- detectability conditions (wind force mical and acoustic pollution, and by Beaufort scale), geographic co- commercial shipping traffic. ordinates, and effort-corrected (days d) The Cariaco Basin, southwest of invested during searches) abundance Margarita and Cumaná, including and sighting indices (APUE and the Cariaco Gulf (approximate SPUE, respectively). area 3889 km2): Although one por- Additionally, an inference of bio- tion of this area has National Park mass consumption was done using the status (The Mochima National species biomass estimates (maximum

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Table 1 Odontocetes cetacean’s records (1997-2008) incorporated in the analysis: Sighting per unit of effort (SPUE), Abundance per unit of effort (APUE), Biomass (kg), according to Trites & Pauly (1998), and *Barlow et al. (2008), Total Prey Biomass Consumption (PBC) in Ton/km2/Year. Common name Scientific name SPUE APUE Biomass PBC Common dolphin Delphinus sp 0.59 17.78 80* 9734.82 Atlantic spotted Stenella frontalis 0.28 4.84 67.50 5301.40 dolphins Common bottlenose Tursiops truncatus 0.16 1.56 203 1709.27 dolphin Guiana dolphin Sotalia guianensis 0.10 2.87 38.60 3138.11 Pantropical spotted Stenella attenuata 0.06 0.74 71,70 814.57 dolphin weight) developed by Trites & Pauly using gaussian kriging interpolation. (1998), and updated by Barlow et al. Biomass consumption by species (2008). Then, following the approach was also plotted, with details on the of Read & Brownstein (2003), the esti- proportion of sardines in their cor- mates were incorporated to the expres- responding diet. Confidence inter- sion: IB (Ingested Biomass) = 0.123M vals of total biomass consumption 0.80. Subsequently, the ingested biomass by species were obtained through a was extrapolated to the density calcu- non-parametric bootstrap. Statistical lated through the APUE, using the ap- differences between species biomass proximate total areal extension of NE consumption estimates were estab- Venezuela (30000 km2), over a time lished by Kruskal Wallis test, concur- frame of a year. The relative propor- ring with the non parametric distribution of small pelagics in the diet was tion of the sample (Zar, 1996). approximated after Pauly et al. (1998), for common dolphins, the proportion RESULTS was modified after the diet information in Naveira (1996). Odontocete occurrence Using the geo-statistical analysis tool of ArcGIS 9.2, maps of prey From all the odontocete species biomass consumption density were observed off the NE coast of Venezu- done for species with a SPUE > 0.15. ela during 1997-2008 (Table 1), the The maps were constructed using the majority of the observations corre- biomass consumption estimates, ef- sponded to the local form of the com- fort-corrected APUE and geographi- mon dolphin (Delphinus spp.), fol- cal coordinates as input parameters, lowed by Atlantic spotted dolphins. interpolated on a 1.8 × 1.8 km grid The dominance of Delphinus spp.

Rev. Mar. y Cost. ISSN 1659-455X. Vol. 1. 245-257, Diciembre 2009. 249 Lenin E, Oviedo Correa encounters was reflected particularly the south-eastern coast of Margarita in both, the sighting (SPUE) and the Island and the continental coast of relative abundance (APUE) indices. central Paria Peninsula, 2) the western side of the Araya Peninsula. At- Biomass consumption distribution lantic Spotted Dolphins concentrated their prey biomass removal by preda- The biomass consumption of all tion to the deep waters of the north- five species is presented in Table 1 eastern portion of the shelf edge, and and illustrated in Figures 2 and 3. the western side of Margarita Island The data shows the differences in toward the Cariaco Basin. The mod- habitat use by species, tendency that el also showed that spotted dolphin was supported statistically (Kruskal consumption increased progressively Wallis, X2: 14.84 DF: 3, p < 0.05). from the shelf’s edge to deeper waters Common dolphins, which were dom- south-west of La Blanquilla Island. inant in the study area, presented a Bottlenose dolphins increased their greater level of consumption within level of prey removal in the eastern shelf waters. The prey biomass con- coast of Margarita Island, and around sumption pattern of S. guianensis deep waters off the shelf toward the remained confined to coastal waters, central coast of Venezuela. in contrast to Stenella dolphins that removed prey biomass located along DISCUSSION the shelf’s edge and off deeper, transitional waters. Common bottlenose Ecological niche as described in dolphin prey biomass intake was here, refers to the biotic and abiotic considerable at mid-shelf waters, not conditions in which a species is liv- close to the continental coastline, ing, that particularly includes the but to Island archipelagos within the resources it consumes and the way shelf ecosystem. it exploits them (Pianka, 1974). The The distributions of the biomass feeding niche as a subset of the eco- consumption pattern agrees with the logical niche would be framed by trend described above (Figures 3-6); three major dimensions intercon- biomass removal by common dol- nected: the trophic dimension includ- phins was mainly concentrated in ing diet composition by prey taxa shelf waters, covering also the deep - prey length, the spatial dimension, waters of the Cariaco Basin. Biomass with the definition of discrete feeding consumption by common dolphins is areas (which implies feeding depths) comprised by an important proportion and the temporal dimension. Behav- of small pelagics (60%). The highest ioral traits relative to foraging success level of consumption was localized in are also considered as a key essential two key areas: 1) the waters between element for foraging niche definition.

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Figure 2

Prey biomass consumption levels by species: Filled circles correspond with common dolphin (light gray), Pantropical spotted dolphins (medium light grey), and Atlantic spotted dolphin (dark grey), small gray filled circles with concentric dot represent Guiana dolphins, and blank unfilled circles common bottlenose dolphins. Circle size is proportional to the level of biomass consumption.

Figure 3

Prey biomass consumption levels by species (solid bar) with details of representative proportion of small pelagic consumed (patterned bar): Common dolphin (60%), Pantropical spotted dolphins (10%), Atlantic spotted dolphin (10%), Guiana dolphins (30%), and common bottlenose dolphins (20%).

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Figure 4

Prey biomass consumption by common dolphin (Delphinus sp), levels on consumption are represented by light gray to the lowest, and dark gray to the highest level of biomass removal.

Figure 5

Prey biomass consumption by Atlantic spotted dolphin (S. frontalis), levels on consumption are represented by light gray to the lowest, and dark gray to the highest level of biomass removal.

252 Rev. Mar. y Cost. ISSN 1659-455X. Vol. 1. 245-257, Diciembre 2009. Patterns of prey biomass consumption by small odontocetes in the northeastern coast of Venezuela

Figure 6

Prey biomass consumption by common bottlenose dolphin (T. truncatus), levels on consumption are represented by light gray to the lowest, and dark gray to the highest level of biomass removal.

The distribution of biomass consump- by Freon et al. (1997) as key fishing tion by odontocetes, based on the rel- grounds (areas 2 and 6; Figure 1). ative abundance of toothed cetacean Consequently, locations of common off the northeastern coast of Venezue- dolphin prey biomass consumption la, primarily highlight clear evidence would also coincide with the loca- that predators are not uniformly dis- tion of the most important coastal tributed throughout the environment upwelling area off the coasts of the of the study area; and secondly, the Central Paria and Araya Peninsulas. location of the spatial arrangement of The occurrence of Delphinus spp. predatory patterns concentrate in dis- has been linked with areas of high crete areas, giving insight into habitat productivity; as a result the species use and resource partitioning. has been used as an indicator of up- The predatory pattern illustrated welling waters in the Eastern Tropi- for Delphinus spp. and the prey bio- cal Pacific (Ballance et al. 2006; mass removal within shelf habitat Fernández et al. 2007; Fernandez & represents the close spatial relation Oviedo, 2009). Since predator bio- between predator- prey; particu- mass consumption distribution local- larly with the potential local prey of ly emulated that of its potential prey, common dolphins, round sardinella, and in this specific case, overlapped specifically on the locations referred with areas of coastal up-welling, the

Rev. Mar. y Cost. ISSN 1659-455X. Vol. 1. 245-257, Diciembre 2009. 253 Lenin E, Oviedo Correa spatial arrangement of the preda- In general this approach combin- tory patterns of common dolphins ing elements of spatial and trophic included discrete areas limited by ecology, has established clear pat- boundaries, which defined a system terns of habitat and resources par- diverging by physical and biological titioning, plus trends in occurrence features. dominancy in coastal and shelf areas The trends in distribution of es- of an important portion of the Ven- timated prey biomass removal by ezuela’s exclusive economic zone. odontocetes particularly suggest the However, the information presented differentiation of foraging habitats, here is conditioned by two impor- primarily in shelf waters, with a prey tant limitations: 1) the estimations biomass that is comprised basically of relative abundance are based on by demersal fish and small pelagics a large data set derived from a non- (including S. aurita). Additionally, systematic research effort, and 2) cetaceans inhabiting transitional- the information on diets is not based oceanic depths were associated with on an local empirical evidence, it is a predatory pattern that probably re- based on the diet accounts proposed lies on pelagic - mesopelagic squid by Pauly et al. (1998), therefore it and myctophids. would not yield important local par- According to Pusineri et al. ticularities. (2001), the patterns of trophic segre- Prey biomass consumption distri- gation within the cetacean community bution assumes that predators’ spatial reported here, could be considered as arrangement match that of their prey. an expression of differences in feed- However, prey abundance by itself ing tactics and habitats, similar to the should not be considered as a unique trophic segregation of fin and minke proxy of habitat use, the abundance of whales off the Bay of Fundy, Canada cetacean predators also play a direct (Ingram et al. 2007) and the habitat role, or an indirect pressure through partitioning of dolphins in the mid- “seascapes of fear” (sensu Wirsing et atlantic ridge (Doksæter et al. 2008). al. 2008), in the definition of both the Provided that the spatial distribution spatial and foraging patterns of ceta- of a given predators is conditioned by cean species. the specialized or generalized pattern According to Pauly and Zeller of food consumption, and associated (2003), the spatial trend in regional- with the spatial arrangement of its ization, as the one presented in this prey (Doksæter et al. 2008, Forcada, report represents a key base-line to 2002), the distribution of biomass assess ecosystem health and evaluate consumption by top predators would management scenarios. be an indirect indication of prey location and abundance.

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