Diet analysis of the main cetacean’s species in waters of the North-West Iberian Peninsula and analysis of macro and microplastics in their stomachs
- Autores: Alberto Hernández González
- Directores de la Tesis: Camilo Saavedra Penas (dir. tes.), Graham John Pierce (dir. tes.)
- Lectura: En la Universidade de Vigo ( España ) en 2023
- Idioma: inglés
- Tribunal Calificador de la Tesis: Juan Antonio Raga (presid.), Izaskun Preciado Ramírez (secret.), Alfredo López (voc.)
- Programa de doctorado: Programa de Doctorado en Ciencias Marinas, Tecnología y Gestión por la Universidad de A Coruña; la Universidad de Santiago de Compostela; la Universidad de Vigo; Universidade de Aveiro(Portugal); Universidade de Porto(Portugal); Universidade de Trás-os-Montes e Alto Douro(Portugal) y Universidade do Minho (Portugal)
- Materias:
- Enlaces
- Tesis en acceso abierto en: Investigo
- Resumen
In this Doctoral Thesis we have studied the feeding ecology of several odontocete cetacean species present in the northwest of the Iberian Peninsula, specifically in Galicia. This geographical area is characterised by having highly productive marine waters due to the synergy of several factors, mainly related to the upwelling process. This oceanographic phenomenon occurs mainly in summer, when the northerly wind (nordés) displaces the coastal surface waters towards the open ocean and they are replaced by deep and cold nutrient-rich waters. As a result of this seasonal water renewal, the Galician marine ecosystem presents a great level of biodiversity (at least 31 species of marine mammals, 398 species of fish, and 75 species of cephalopods) and therefore supports a high fishing activity (around 4,000 vessels with fishing license in Galicia).
Among the wide variety of marine mammals observed in Galicia, the most frequently observed are: the common dolphin (Delphinus delphis), the striped dolphin (Stenella coeruleoalba), the bottlenose dolphin (Tursiops truncatus) and the harbour porpoise (Phocoena phocoena). As top predators, all these small odontocete species could be playing an important role within the Galician marine ecosystem since their populations are able to influence the structure of the food web (e.g. by regulating the diversity and/or abundance of other species, contributing to the resilience of the ecosystem). However, due to the different anthropogenic pressures to which they are exposed to (e.g. bycatch in fisheries, habitat degradation, overexploitation of fisheries resources, pollution, and marine litter), some cetacean populations are declining and have an unfavourable conservation status.
The present study is focused on the analysis of the stomach contents of the 4 odontocete cetacean species mentioned above. In total, 301 stomach contents (226 common dolphins, 18 striped dolphins, 38 bottlenose dolphins, and 19 harbour porpoises) collected from both stranded and bycaught animals over a period of 13 years (2005 - 2018) were processed. In addition, all the information available from previous diet studies, conducted in the same study area, was assembled and combined with the data from the new analyses, increasing the total number of samples analysed to 1007 and extending the time series to almost 30 years (from 1990 to 2018). Hence, for each of the 4 cetacean species studied it has been possible to: describe the diet composition (qualitatively and quantitatively), calculate the relative importance of the different prey species consumed, identify which factors affect their diet variability (e.g. cetacean length, sex, decomposition state, date of stranding, stranding location, or cause of death, among others), and determine if there is competition for resources with fisheries operating in the study area. Parallel to this and within the framework of the stomach content analysis, the presence of microplastics in the stomachs of common dolphins was also examined, which is an emerging global threat to marine fauna in recent years.
To this end, to reconstruct cetaceans diet a direct procedure (or traditional methodology) has been carried out. It consisted of sieving the stomach contents of cetaceans to separate all the diagnostic hard prey structures (mainly otoliths, fish bones, and cephalopod beaks) from soft prey tissues (e.g. muscle tissues). Under the assumption that each taxon (or group of related organisms) has similar diagnostic hard structures (in size and shape), and that these features are different between different taxa, it was possible to identify the preys consumed by cetaceans to the species, genus or family level (depending on the degree of erosion suffered by these structures during the digestion process, or the existence of identification guides). Subsequently, the diagnostic hard structures were measured to reconstruct the original prey lengths and weights by applying regression equations. On the other hand, once all hard prey structures (and parasites) were removed, the soft tissues that were retained in the sieves were digested with 10% potassium hydroxide (KOH) to separate and identify the remaining inorganic elements (microplastics) in the stomach contents of common dolphins.
Chapter 1 presents the results of the analysis of 751 common dolphin stomach contents, which indicate that the diet of this cetacean species is mainly composed of fish (Index of Relative Importance - %IRI = 96) and, to a lesser extent, of cephalopods (%IRI = 4). Once the 257,666 diagnostic hard prey structures were identified, it was observed that the blue whiting (Micromesistius poutassou) is the most important prey in terms of occurrence (%F), number (%N) and biomass (%W), followed by the Atlantic horse mackerel (Trachurus trachurus), the European hake (Merluccius merluccius), and the sardine (Sardina pilchardus). Based on all the diagnostic hard prey structures found in the stomach contents, it was calculated that each individual had, on average, 4 kg of ingested food in its stomach and, applying regression equations to all these structures, the mean prey length was estimated to be 12 cm and the mean prey weight 76 g. Generalised Additive Models (GAMs) were used to explore the effects of several biological, spatial and temporal parameters on the presence of these main prey species. Over the study period, it was observed that the relevance of the sardine in the diet has been decreasing in the last 15 years, which is related to the decline of sardine abundance (Iberian stock). Similarly, an increase in the consumption of European hake was detected over the time series, coinciding with the population growth of the species in the study area. On the other hand, GAMs demonstrated a seasonal pattern in the diet composition of common dolphins, with a higher consumption of blue whiting during summer (between May and September) and gobies (fish of the family Gobiidae) throughout the rest of the year (from October to March), which could suggest seasonal movements of the dolphins between coastal and oceanic waters. Main prey species consumed by common dolphins are also target species for Galician fisheries and, given that 66% and 85% of the average size classes consumed by common dolphins (of blue whiting and European hake, respectively) are above the minimum landing sizes, the results suggest that there is a competition for these resources.
Chapter 2 reveals that striped dolphins diet is mainly composed of fish (%IRI = 88) and, although cephalopod remains appeared in almost half of the stomach contents analysed, their contribution is relatively low (%IRI = 12). In addition to identifying a total of 9237 diagnostic hard prey structures in all the stomach contents analysed (n = 60), crustacean remains (infraorder Caridea) were also recorded in approximately 28% of the cetaceans analysed (n = 18). Each striped dolphin was estimated to have, on average, 2 kg of ingested food in its stomach; being the estimated mean prey length 11 cm and the mean prey weight 56 g. Although little is known about the feeding ecology of striped dolphins in the study area, the results highlight that this species feeds most frequently on blue whiting (%F = 24) and gobies (%F = 27). In addition, GAMs reveal that striped dolphins ingest these two preys seasonally (as common dolphins do), consuming more blue whiting during summer (when the abundance of this fish species is higher) and more gobies throughout the rest of the year. In relation to body condition, it has been observed that leaner animals had higher numbers of cephalopods in their stomachs (Ommastrephidae and Sepiolidae families) than fatter animals, probably related to the low lipid content of cephalopods. Additionally, the results indicate a possible indirect competition with fisheries since the mean length of blue whiting consumed by striped dolphins is below the minimum landing size.
Chapter 3 investigates the diet of bottlenose dolphins through the analysis of 124 stomach contents, which includes a wide variety of taxa from both pelagic and demersal species. The identification of 35,896 diagnostic hard prey structures indicated an essentially piscivorous diet (%IRII = 99) and it was estimated that the stomachs contained, on average, 18 kg of ingested food. Once these hard structures were measured, the mean prey length was estimated to be 24 cm and mean prey weight 409 g. The most important prey is the blue whiting followed by the European hake in terms of occurrence (%F), number (%N) and biomass (%W). GAMs results reveal that the consumption of blue whiting, by bottlenose dolphins, has decreased over the years (from 1990 to 2015). Nonetheless, it is important to highlight that in Galicia there are 2 subpopulations of bottlenose dolphins: a coastal ecotype mainly present in the south of the study area, and an oceanic ecotype mainly occurred in the north of the study area. The results of the present study show that the diet composition of these two subpopulations is different. The diet of the coastal ecotype consists of 68% pelagic prey and 32% demersal prey, while the diet of the oceanic ecotype is predominated by pelagic prey (83%) rather than demersal prey (17%). On the other hand, it should be noted that the samples analysed came from individuals that either died bycaught in fishing gear or died from other causes (e.g. disease), which could produce diet variability. Despite this, no significant differences in diet composition were found between the two causes of death. Taking into account the length of the preys comsumed, it seems that bottlenose dolphins compete directly with the fisheries in Galicia for blue whiting and European hake, as both exploit the same size ranges.
Chapter 4 shows the results of the analysis of 72 harbour porpoise stomach contents from the Iberian population. It is important to point out that this is a population genetically isolated from the rest of the European populations and it is in risk of extinction. The 6411 diagnostic hard prey structures identified suggest a mainly piscivorous diet (%IRI = 99). Once all these structures were measured it was calculated that, on average, 2 kg of ingested food were present in each of the stomachs analysed; the mean prey length was estimated to be 16 cm and the mean prey weight 54 g. The most important prey are, in this order, pouting (genus Trisopterus), blue whiting, Atlantic horse mackerel and European hake. After assessing which variables may affect the presence of these prey species in harbour porpoise stomachs through GAMs, the results indicated an ontogenetic variability in the diet composition, i.e. juvenile animals consume more pouting (a shallow-dwelling species), while adult animals consume more pelagic prey (e.g. blue whiting, Atlantic horse mackerel and European hake). Interannual variation in the diet was also detected, with an increase in the European hake consumption over the years (from 1990 to 2018) probably due to an increase in the spawning stock biomass of the species in the study area. The results also suggest a competition with fisheries in the area, since 28%, 51%, 79%, and 35% of the size classes of the main prey species consumed by harbour porpoises (pouting, blue whiting, Atlantic horse mackerel, and European hake; respectively) are above the landing size classes. However, given the small Iberian population of southern harbour porpoise (of approximately 3000 individuals), the total estimated consumption of these 4 main prey species is around 10% of what is fished by the Portuguese and Spanish fleets in waters off the west coast of the Iberian Peninsula.
In Chapter 5 the stomach contents of 35 common dolphins stranded between 2005 and 2010 were processed to investigate, for the first time in the Iberian Peninsula, the presence of microplastics (plastic items smaller than 5 mm in diameter) in the stomachs of this cetacean species. Eliminating the fibres, that may come from airborne contamination from textile fibres, a total of 411 microplastics were identified, 12 microplastics on average per stomach content, in 94% of the individuals analysed. The microplastics were classified as: fibres (96.6%), fragments (3.2%) and beads (0.2%). The colours most frequently observed were blue and black. Only one macroplastic was detected within all samples analysed: a red filament of 6.8 mm long. In this respect, the quantities and volumes of microplastics present in the stomachs analysed do not appear to be able to cause physical harm to the common dolphins (e.g. blockage of the digestive tracts), however, it cannot be ruled out that the possible contaminants adsorbed on the surface of microplastics may be released and accumulated in the tissues of the individuals (causing long-term toxic effects).
Combining all the results of this study we can obtain a general picture of the feeding ecology of the 4 small odontocete cetaceans species analysed. In a nutshell, we can say that common dolphins, striped dolphins, bottlenose dolphins and harbour porpoises are mainly piscivorous and that blue whiting is one of the most important prey species in their diet (in occurrence, number and/or biomass) and also one of the most important economic fisheries resources in Galicia. Hence, blue whiting is a key species to understand the role of these top predators in Galician waters. In more broad terms, stomach contents suggest that common dolphins and striped dolphins (both mainly oceanic cetacean species) feed predominantly on pelagic species (e.g. blue whiting, Atlantic horse mackerel, and gobies) over the continental slope zone, although they may occasionally feed on demersal species (e.g. European hake, squids ¿ of genus Loligo and genus Alloteuthis) in neritic waters of the continental shelf. Other locally abundant fish species such as pouting (family Gadidae) also contributed substantially to the diet of harbour porpoises (coastal cetacean species), indicating that this cetacean species prefers to feed on shallow areas (30 - 100 m depth). The information on bottlenose dolphin diet shows a more complex feeding behaviour since the high diversity prey species identified in the stomach contents implies movements over the entire continental shelf, from the coast to the edge of the slope. It was also found a high degree of overlap in diet composition between bottlenose dolphins and harbour porpoises, and therefore, competition for food resources among these two sympatric cetacean species might occur. However, there are indications of a possible dietary partitioning (or spatial segregation in foraging), since differences in the prey sizes were also found; i.e. bottlenose dolphins tend to feed on larger prey (> 20 cm) than harbour porpoises (< 20 cm).
It should be noted that the long time series analysed (almost 30 years) and the large number of samples available (1007 stomach contents in total) allowed us to detect, at a regional level, how changes in the abundance of prey populations are reflected in the diet composition of cetaceans. As an illustration, for example, the decrease of sardine biomass in Galician waters over the years was reflected differently in the diet of the 4 small odontocete cetacean species: in the case of the common dolphin sardine is no longer one of the main prey species, in the case of the striped dolphin and harbour porpoise it has been consumed less frequently, and in the case of the bottlenose dolphin its consumption has ceased.
It must be taken into account that this thesis, while describing the feeding ecology of these 4 small odontocete cetacean species and their possible interactions with fishing activity, it also provides quality information that can be integrated in ecosystem models for fisheries assessment. These models are used to describe and quantify the biomass flow between the different trophic levels and species of the Galician marine ecosystem (top predators ¿ fish/prey - fisheries). This knowledge about the functioning of the marine ecosystem may be very useful to predict the consequences of disrupting any of the flows between groups or levels and, therefore, are highly valuable to report on the suitability of different management decisions.
Variations in cetacean diet can provide information on changes in the trophic levels, which is an indicator of the ecosystem health. In this line, the OSPAR Convention for the Protection of the Marine Environment of the North-East Atlantic assesses the state of the food webs in the Bay of Biscay through the indicator FW4 (Changes in the average trophic level of marine predators), which could be fed by the information provided in this thesis. Similarly, the diet composition of cetaceans present in Galicia also could provide valuable information for Descriptor 4 (D4 - food webs) of the Marine Strategy Framework Directive, since it is an important parameter defining the trophic relationships of top predators within the ecosystem. Besides, information on microplastics, obtained from the stomach contents of common dolphins, is also useful to address the Criteria 3 (C3 - monitoring and assessment of the amount of micro-litter ingested by marine species) of Descriptor 10 (D10 - Marine litter). Therefore, all the information generated in this thesis, on cetaceans feeding ecology and some anthropogenic impacts (i.e., microplastics), has the potential to be used and integrated to respond the requirements of different legislations at national and international levels.
