S12.5: Trawler discards: a threat or a resource for opportunistic seabirds?

Human fisheries and seabirds when foraging share the same habitat, the sea, and they are looking for the same goal, marine organisms, especially fish. Since seabirds and fisheries occupy the same ecological niche and consequently they share food webs, their interactions are extremely diverse and seabirds and fisheries performances may be favoured or threatened by the activity of the other. Duffy & Schneider (1994) listed several positive and negative interactions from the point of view of both seabirds and humans. The most severe positive interactions are for humans an increase of fishery through location of prey or through fertilising waters by guano run-off, and for seabirds the exploitation of discards and offal, whereas human fishery landings may be negatively affected by seabird consumption and seabird adult mortality increased from fishing nets ands lines (see also Furness & Ainley 1984; Nettleship et al. 1984). These interactions may be very frequent because fish-consumer seabirds are especially abundant in regions were primary production is high and consequently fish populations are large, and fisheries are especially important in these areas, where commercial yields are greater (e.g. upwelling regions: the Benguela Current, the California Current, the Humboldt Current).

In the Mediterranean Sea, where primary production is lower than in most of the open oceans, neither seabirds nor fisheries are so abundant (Farrugio et al. 1993; Oro & Ruiz 1997), but some interactions occur and they probably coincide with those recorded in these areas. Relationships between trawlers and seabirds seem to be restricted to a foraging resource for scavenging seabirds (Fasola et al. 1989; Oro & Ruiz 1997), with no detrimental effects on adult survival such as those caused by hooks of fishing lines used by other fleets (Guyot 1988; Oro 1998). From the point of view of trawler fleet, fish stock consumed by seabirds has not yet been estimated, but this consumption probably has no great effect on fishery landings (Ruiz et al. 1996, although see Furness & Ainley 1984). It is well documented that around the Ebro Delta, in western Mediterranean, opportunistic seabirds exploit discards from fisheries, especially trawlers (Oro & Ruiz 1997), and that trawler discard availability improve the breeding performance of at least large gulls such as Yellow-legged Gulls Larus cachinnans, Lesser Black-backed Gulls L. fuscus or Audouin's Gulls L. audouinii (Oro et al. 1996a and references therein). Around this area, the large width of the continental shelf and the nutrients carried by the Ebro River yield one of the most important areas of primary production and consequently of fishing grounds in the whole Mediterranean (Palomera. 1992; Palomera & Pertierra 1993; Estrada 1996). As expected, the number of fishing vessels is high, especially trawlers, which concentrate here the largest trawler fleet in Catalonia and one of the largest in the whole Mediterranean (Charbonnier & García 1985; Martín 1989 and 1991; Álvarez 1990). This paper deals with the relationships between trawlers and opportunistic seabirds in the Ebro Delta, focusing on the benefits and the threats from the seabird perspective. A multispecific seabird colony take advantage of discards from trawler vessels, whereas overexploitation of fish stocks in the Mediterranean and also in this area occurs during the last decades (FAO 1993; Safina 1995; Anonymous 1996), and this can have a negative impact by reducing natural food availability for seabirds breeding there. In fact, a trawling moratorium has been established since 1991 around the Ebro Delta to allow fish populations for recovering their numbers from overfishing. This moratorium lasts two months each year and it overlaps with the reproductive season of seabirds breeding there, with important effects on their feeding and breeding ecology (Oro et al. 1995; Oro 1996b; Oro et al. 1996a and b; Oro et al. 1997). Up to now, trawler discard availability had been considered a positive factor for seabird populations since it allowed an increase of breeding numbers, but if overfishing occurred, this trend could be reversed and trawler activity should be considered a threat rather than a resource for opportunistic seabirds.

Data have been collected between 1992 and 1997 in a multispecific seabird colony on the Punta de la Banya (Ebro Delta Natural Park, NE Spain: 40º37’N, 00º35’E). Main species breeding here in order of reproductive numbers are Audouin's Gull, Yellow-legged Gull, Common Tern Sterna hirundo, Sandwich Tern S. sandvicensis, Slender-billed Gull L. genei and Lesser Black-backed Gull (see Table 1), and data on the ecology of these species are presented here. All these species exploit discards from trawlers (Oro & Ruiz 1997). Some biological parameters were recorded depending on the species and years, basically breeding numbers, clutch size, average egg volume in a clutch and breeding success. Data on breeding numbers from previous years was collected from unpublished literature (years 1980, 1988 -Albert Martínez, unp. data- and from 1993 to 1997 -Daniel Oro & Albert Martínez, unp. data-) and included in the analysis of energy requirements for seabird community and energy availability from fish discarded (see below). Other species breed only intermittently such as Black-headed Gull L. ridibundus or have small breeding numbers, such as Little Terns S. albifrons or Mediterranean Gull L. melanocephalus (Oro 1996c), and are not considered here, even although most of them may also exploit discard from trawlers (Oro & Ruiz 1997). Finally, some Procelariforms such as Cory’s and Balearic Shearwaters (Calonectris diomedea and Puffinus yealkouan respectively) are known to forage naturally around the Ebro Delta and to exploit discards from trawlers to a large extent in this area (Abelló & Oro 1996; Oro & Ruiz 1997 respectively) but they do not breed here and ecological parameters of these species are not available.

In relation to trawler activity, data on the amount of fish discarded as a function of fish landing was collected between 1992 and 1997 (see details in Oro & Ruiz 1997). Statistics of fish catches from fishermen’s guild bulletins were collected since 1973 to 1995 at Sant Carles de la Ràpita, the largest harbour for trawlers in the area (60% in numbers, 74% in total power, HP) and the closest to the colony. Landings were separated into two groups, one formed by clupeoids, since they constitute the main prey for most of the seabirds breeding there, and the other by the rest of marine organisms including other fish species, cephalopods, crustaceans and molluscs. Trend of landings through the years was assessed with the lowess fit method, which produces locally weighted regression smoothing using an iterative weighted least-squares method (Cleveland 1979). Time series of fishery landings can provide important indications of changes in a fishery, or changes to the underlying environment. In the Mediterranean, this is essential since complete or independent information such as on the fishing intensity or fishing mortality affecting fishing populations is normally lack. This information can indicate if overexploitation occurs in the area, affecting availability of fish for seabirds breeding there.

Energy available from trawler discards and energy requirements of seabirds breeding at the Ebro Delta were estimated in order to assess if during the last 20 years the relationship between energy available and energy requirements has changed as a results of variations in fishery catches and/or colony size. Landings over the years were used to estimate energy available from the amounts of fish discarded from trawlers during a breeding season using the correlation calculated by Oro & Ruiz (1997) and assuming that during the period considered (1980-1997) this correlation did not vary. Energy requirements of the colony were estimated using the number of breeding pairs throughout this period and the field metabolic rate for each species at each year (see also Bryant & Furness 1995; Garthe et al. 1996).

Effects of trawler discard availability were diverse and they depended on the seabird species (Table 2). The species less affected by the changes in trawler activity through the moratorium seemed to be Slender-billed Gulls and Sandwich Terns. For some species such as Audouin's Gulls, breeding success was positively associated to food availability through trawler discards (Fig. 1). Trawler fishing yield on clupeoids in the Ebro Delta area has showed some fluctuations, very similar for both Sardine Sardina pilchardus and Anchovy Engraulis encrasicolus, but it has decreased as a whole during the last 20 years, especially since 1987 (Fig. 2). A similar trend was recorded for the other marine organisms, with an increase of yields during the 1980s and a further decreased during the 1990s (Fig. 2). As a result of the decrease in fishery landings, energy available from trawler discards between 1980 and 1997 decreased as well, whereas the size of the multispecific seabird colony has greatly increased during the same period (Fig. 3). An index between energy available and energy requirements for the seabird community showed that this ratio has decreased throughout the years, although actually energy available is still ca. two times greater than energy requirements (Fig. 3).

The Ebro Delta area is one of the most important fishing grounds for cupleoids in the Mediterranean (Pertierra & Castellón 1987; Palomera 1992; Garcia et al. 1995; Maynou & Palomera 1995; Palomera et al. 1995). This fact has allowed the development of a large fishing fleet (Martin 1989; Irazola et al. 1996; Oro & Ruiz 1997) and probably has enhanced the establishment of a large seabird breeding population, after the protection of the area as a Natural Park in 1986. Protection of breeding grounds from human disturbances was also an important factor for seabird population growth especially during the 1980`s, when a strong immigration process to this site occurred probably from other colonies. After this immigration process, large food availability from trawlers influenced high breeding success, high recruitment rates and rapid accession for breeding (author, unpubl. data). In 1991 a trawling moratorium was established around this area to recover fish populations, although economic factors rather than biological factors were taken into account when determining the length and the dates of the closed season (Lleonart & Recasens 1996; see also Masood 1997). Since then, the trawling moratorium has lasted two months each year, always during spring and therefore overlapping with the breeding season of seabirds reproducing there (Oro et al. 1996a and b). Since the period of moratorium has changed each year (April-May, May-June, or June-July depending on the years) and breeding phenology of each seabird species is different (soonest for Yellow-legged Gull, latest for Slender-billed Gull and Sandwich Terns, broadest for Common Terns), effects of trawling discard availability on different breeding parameters for each species could been assessed between 1992 and 1997. Already in 1991, the first year of trawling moratorium, a dramatic decrease of breeding success in Audouin's Gulls was recorded in the Ebro Delta and at the neighbouring Columbretes Islands colony, also affected by the closed season (Paterson et al. 1992). Latter, several studies confirmed that breeding success and other breeding parameters of Audouin's Gull decreased significantly when trawling moratorium was established, and that other species such as Yellow-legged and Lesser Black-backed Gulls were also affected by the closed seasons (see Table 1 and references therein). Oro & Ruiz (1997) listed all the species that followed trawlers (all the breeding species except Little Terns), and those that had higher success exploiting discards from trawlers at this area, such as Audouin's Gull. Effects of discard availability on breeding parameters were important especially for larger and abundant species, for less specialized foragers and for those with large foraging range such as large gulls and Common Terns, although adult survival was not affected at least in Audouin's Gull (Oro et al. 1997). All this information showed that the relationship between opportunistic seabirds and trawlers was very strong at the Ebro Delta, and that the closed seasons were a threat especially for endangered species, such as Audouin's Gull (Lambertini 1995 and 1996; Oro et al. 1996a). In this area, up to 45% of total fish catches are discarded by trawlers, and estimates suggest that discards may readily support all scavenging seabirds and their energy demands for breeding (Oro & Ruiz 1997). However, the increase in seabird breeding numbers and the decrease in fishing catches in recent decades may reverse this situation.

The key point for seabird population dynamics at the long term in the Ebro Delta colony is whether substantial changes in fish stocks (especially cupleoids, the main prey for most of the seabird species breeding there) have occurred due to fishery overexploitation. Only fishery landings throughout the years may indicate some trends in fish populations, in the absence of stock assessments or surveys over the time, although influence of changes of the environment or the ecosystem cannot be distinguished from those caused by fishing (Fiorentini et al. 1997). Opposite to that recorded in the North Atlantic and North Pacific, fishery landings in the Mediterranean did not show a peak in the 1970’s and 80’s, but a sustained trend in production during the last decades. It seems likely that overexploitation has occurred for some species and in some areas, although production has been maintained in the Mediterranean as a whole because of the increase of runoff of thousands of tons of nutrients, especially for plankton feeders such as cupleoids (FAO 1992; Caddy et al. 1995). However, sustained trends in production do not necessarily mean large and stable fish populations, as recorded in the Black Sea, another semi-enclosed sea like the Mediterranean, where a precipitous collapse of fish populations occurred after years of sustained landings (Safina 1995; Prodanov et al. 1997). Another problem to assess population trends for clupeoids is that this group is distinguished by the great fluctuation in the size of their populations due to their short lifespan and their dependence on the lowest trophic levels (phytoplankton and zooplankton) (Blaxter & Hunter 1982; Pertierra 1992). This natural fluctuation results in greater susceptibility of these populations to intense fishing (Pertierra 1992; Irazola et al. 1996). To partially overcome these problems, fishery landings at a smaller scale may be more suitable for assessing trends. Landings of Anchovy in the northwestern Mediterranean have decreased especially since 1983 (Demestre et al. 1987) despite the increase in fishing effort and a similar trend has been observed in the present study when only the Ebro Delta area was considered (Fig. 2). The same trend is observed for Sardine, although it seems that for this species the decline is caused by a decrease in market demand and consequently a decrease in fishing effort by fishing vessels, which probably has allowed this species to recover its populations (Anonymous 1996). Direct methods such as acoustic surveys and indirect methods such as length cohort analysis have recently been carried out in the northwestern Mediterranean to evaluate coastal pelagic biomass and population dynamics of clupeoids. These analyses showed that the biomass of sardine increased in recent years (Miquel & Alvarez 1990; Abad et al. 1990; FAO 1993; Iglesias et al. 1995; Anonymous 1996), whereas the situation for the Anchovy is more fragile probably owing to its high demand, and both spawning and stock biomass seems to decrease (Giráldez & Abad 1991; Palomera & Pertierra 1993; Iglesias et al. 1995; Pertierra & Lleonart 1995; Anonymous 1996). Thus, it seems that at the Ebro Delta area, availability of Sardine, the commonest clupeoid species in this area, may support at least partially the energy requirements of breeding seabirds, whereas consumption of Anchovy may be threatened by overfishing. In the next future, fishery policies of the European Community will probably cause a decrease in the availability of discarded fish for opportunistic seabirds: closed seasons, reduction of fleet numbers or fishing effort, minimum landing size through changes in net mesh size, and use of non commercial fish species can be some of the measures adopted to allow fish populations to recover and to rationalize the exploitation of sea resources. In the North Sea, fishery regulations has occurred over the last 20 years, such as increase of offal retention, increase of net mesh size by 25% or decrease of the minimum landing fish size (Furness 1992). As a consequence, availability of offal has declined since 1970 by at least 50%, and a decrease in seabird numbers are expected, as well as an alteration of seabird community structure (Furness 1992). In northwestern Mediterranean, a trawling moratorium was already established between 1961 and 1965 because of overfishing, and it seems that the moratorium was successful to recover fish populations (Suau 1964; Anonymous 1996). Up to now, few attempts have been made to assess the effectiveness of the trawling moratorium on fish populations (Martin 1995). From this point of view, monitoring seabird numbers and their diet may help to assess whether trawling moratorium is effective or not (Furness et al. 1993; Montevecchi 1993; Furness & Camphuysen 1997). As suggested by Furness (1992) in the North Sea, if fishery regulations and policies ensure the future of fish populations, conservation of seabirds at the Ebro Delta will be in turn favoured, in spite of the decrease of breeding success caused by the changes in fishery trends.

I thank all the people involved in the Audouin's gull research project over the years, especially Meritxell Genovart for her help with the field work, and Paola Dias, Albert Martínez-Vilalta and Xavier Ruiz for their support. Research funds were provided by Instituto para la Conservación de la Naturaleza ICONA, P.N. del Delta de l’Ebre, Direcció General del Medi Natural (Generalitat de Catalunya), Comissionat per a Universitats i Recerca (grants ACOM92/3051/10 and 1996BEAI200023), and the European Science Foundation (Program in Population Biology).

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Table 2 continued.