Estimating Mortality of Black-Browed Albatross

Polar Biol DOI 10.1007/s00300-015-1747-3

ORIGINAL PAPER

Estimating mortality of black-browed albatross (Thalassarche melanophris, Temminck, 1828) and other seabirds in the Argentinean factory trawl ﬂeet and the use of bird-scaring lines as a mitigation measure

1 1 2,3 Leandro Luis Tamini • Leandro Nahuel Chavez • Marıá Eva Gońgora • 4 5 6 Oliver Yates • Fabiań Leandro Rabuffetti • Ben Sullivan

Received: 21 October 2014 / Revised: 21 May 2015 / Accepted: 23 June 2015 Ó Springer-Verlag Berlin Heidelberg 2015

Abstract Seabird bycatch represents one of the main we identified black-browed albatross mortality rates of threats to vulnerable seabird populations, particularly 0.013 and 0.093 birds/haul for net entanglement and cable albatross and petrels, and requires urgent conservation collision (corpses hauled aboard), respectively. From management interventions at a global scale. We studied counts of birds killed or injured by cable collisions, we seabird mortality associated with demersal factory trawl estimate a black-browed albatross mortality rate of 0.237 vessels that target Argentine Hake Merluccius hubbsi along birds/h. We use official fishing effort data to consider the the Argentine Patagonian Shelf and tested the efficacy of potential scale of seabird mortality for the entire fleet and bird-scaring lines as a seabird bycatch mitigation measure. identify the main factors contributing to seabird mortality From November 2008 to June 2010, dedicated seabird in this fishery. Bird-scaring lines eliminated seabird mor- observers recorded three sources of seabird mortality: tality caused by collisions with trawl cables and are rec- entanglements with the trawl net; collisions with the trawl ommended as a short- to medium-term measure to mitigate cables (corpses hauled aboard); and collisions with trawl seabird mortality in this fishery. cables (birds observed killed or injured). During 141 days and 389 hauls, we recorded 17 seabird species associated Keywords Incidental capture Á Mitigation measures Á with vessels, ten of which interacted with fishing gear. The Thalassarche melanophris Á Patagonian Shelf Á Hake most vulnerable species was the black-browed albatross fishery (Thalassarche melanophris). From 41 recovered corpses,

& Leandro Luis Tamini Introduction [email protected] Seabird mortality in fisheries has been recognised as a 1 Albatross Task Force Argentina, Programa Marino, Aves global conservation concern in marine ecosystems Argentinas/AOP, Matheu 1248, C1249AAB Buenos Aires, Argentina (Brothers et al. 1999). Studies have reported high incidental mortality rates associated with different fishing gear, 2 ´ ´ Subsecretarıa de Pesca, Ministerio de Agricultura, Ganaderıa, including gill nets, drifts nets, trawl nets, and longlines Bosques y Pesca de la Provincia del Chubut, Vachina 164, 9103 Rawson, Chubut, Argentina (e.g. Jones and DeGange 1988; Brothers 1991; Weimer- skirch et al. 1997; Sullivan and Reid 2002; Tamini et al. 3 Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia, Julio A. Roca 115 1°, 9100 Trelew, Chubut, 2002;Go´mez Laich et al. 2006; Gonza´lez-Zevallos et al. Argentina 2007). The impact of longline fishing on seabird popula- 4 BirdLife International Marine Programme, RSPB, The tions was only recognised during the last decade of the Lodge, Sandy, Bedfordshire SG19 2DL, England, UK twentieth century (Bartle 1991; Nel et al. 2002), and a 5 Departamento de Conservacioń, Aves Argentinas/AOP, review of the scale of bycatch estimates suggests ca. Buenos Aires, Argentina 160.000 (and potentially in excess of 320,000) seabirds 6 BirdLife International Marine Programme, 44 Quayle Street, become hooked and drown on longlines every year (An- Sandy Bay, TAS 7005, Australia derson et al. 2011). This mortality occurs because seabirds 123 Polar Biol are attracted to vessels by the presence of bait deployed on The main components of a BSL are the supporting line hooks or fish and offal discarded during fishing operations. (backbone), streamer lines and mounting or attachment The magnitude of this mortality is sufficient to consider pole, although BSL designs differ between fisheries that it is responsible for the decline of several threatened (Brothers 1995; Brothers et al. 1999). A mechanized seabird populations (BirdLife International 2004). deployment and retrieval reel is not essential, but may help The first records of seabird mortality in trawl fisheries eliminate BSL entanglements and manual labour (Brothers were reported by Bartle (1991), but received less attention 1995). More recently, more precise recommendations have as the large numbers of seabirds caught on longline hooks been incorporated including: streamers should be brightly was a more readily identifiable impact on populations than coloured and reach the sea surface in calm conditions, mortality associated with trawl gear (Weimerskirch et al. streamers should be placed at intervals of no more than 2000). In trawl fisheries, birds are attracted by fish and 5 m, and a suitable towed device should be used to provide offal discards, and once the birds are in close proximity to drag, maximise aerial extent and maintain the line directly the vessels, mortality occurs due to collisions with trawl behind the vessel during crosswinds (ACAP 2013a). The cables (metal cables used to tow fishing nets), ‘‘third wire’’ aerial coverage and the position of the bird-scaring line are or net sonde cable (a cable that tows a device used to the most important factors influencing their performance monitor nets during fishing) or by entanglement in the nets (ACAP 2013a). (Weimerskirch et al. 2000; Gonza´lez-Zevallos and Yorio Several studies in demersal longline fisheries have 2006; Sullivan et al. 2006b). Impacts with trawl cables demonstrated a significant reduction in seabird collisions occur when birds are in the air or on the water and increase and captures using BSLs (Løkkeborg 2003; Melvin et al. as a function of cable visibility (e.g. material, diameter), 2004c; Reid et al. 2005) and pelagic longline fisheries aerial extent (e.g. a larger aerial extent implies greater risk (Boggs 2001; Melvin et al. 2004b, d). For trawl fisheries, to of collision), the position of discharge in relation to the protect both trawl cables and thus reduce seabird collisions, water entry point of cables, type of discharge (e.g. whole Sullivan et al. (2004) used two BSLs and no mortalities fish vs. viscera) amongst other factors (Dietrich and Melvin were recorded during trials in the Malvinas (Falkland) 2007). The net sonde cable was banned in several fisheries Islands finfish trawl fishery. Melvin et al. (2004a) tested in the southern hemisphere in the early 90 s due to the high single and paired BSLs in the Bering Sea Pollock trawl albatross mortality associated with this device (Bartle fishery and found that both configurations virtually elimi- 1991; Weimerskirch et al. 2000). More recently the impact nated seabird air and water collisions with the third wire. of trawl cables has been shown to cause mortality in a large More recently, Maree et al. (2014) demonstrated not only number of seabird species. Long-winged birds like alba- the effectiveness of BSLs at preventing seabird collisions tross and giant petrels appear to be the most vulnerable as with trawl cables, but following the introduction of BSLs a they forage with outstretched wings, which makes them reduction of [90 % of seabird mortality was maintained particularly susceptible to cable strike (Sullivan et al. over the course of 5 years in a South African trawl fishery. 2006b). Assessing mortality associated with trawl cables is Respectively, 17 and 22 seabird species breed on the complicated as mortality can be cryptic, as not all carcasses coast of Patagonia and Malvinas (Falkland) Islands (Yorio are hauled aboard. Therefore, dedicated seabird observers et al. 1998; Woods and Woods 2006) and more than 50 are required. Currently, interactions with trawl cables are seabird species forage on the Patagonian Shelf (Favero and not included in traditional observer data collection proto- Silva Rodriguez 2005) representing an area of global sig- cols (Moore and Zˇ ydelis 2008) which hinder the develop- nificance. More than 67 % of c. 602,000 pairs of the black- ment of an accurate estimate. browed albatross breeding population reproduce in the Mitigation measures can be defined as the modification Malvinas (Falkland) Islands and use the shelf for foraging to fishing practices and/or equipment that reduces the (Gales 1998; Huin 2002). This species has been downlisted likelihood of incidental seabird bycatch (Brothers et al. from endangered to near threatened according to IUCN 1999) and are also relevant for other species of mega fauna, criteria (BirdLife International 2014b) due to the recovery particularly marine mammals and sea turtles (for reviews of breeding populations in the Malvinas (Falkland) Islands, see Rowe 2007; Lucchetti and Sala 2010). Streamer lines which were previously estimated to be in significant are known by a variety of names, including: bird-scaring decline (Gales 1998; Huin 2002). However, the South lines (paired and single), tori lines, tori pole streamers and Atlantic supports several major fisheries with evidence of bird lines or BSL by the initials (Bull 2007) and were mortality of this species associated with net sonde cable, initially used for longline fisheries and later adapted for trawl cables and nets (Gonza´lez-Zevallos and Yorio 2006; trawl vessels. Brothers et al. (1999) define a BSL for Sullivan et al. 2006b; Gonza´lez-Zevallos et al. 2007; longline fisheries as any device that, when deployed astern Favero et al. 2011), and further efforts are required to during line setting, deters birds from taking baited hooks. identify and mitigate seabird mortality in the region. 123 Polar Biol

In this paper, we present information on seabird interactions with factory trawlers targeting Argentine Hake (Merllucius hubbsi). Our objectives include: (1) deter- mining the species composition and the relative abundance of seabirds attending vessels, (2) evaluating the factors that affect the collision of seabirds with trawl cables in the fleet, (3) estimating the scale of seabird mortality caused by collisions with trawl cables in this fleet and (4) examining the efficiency of mitigation measures for these vessels.

Materials and methods

Study area and ﬂeet characteristics

The Patagonian Shelf ecosystem extends from Uruguay to the Isla de los Estados and the Burdwood Bank. It has a total area of about 2.7 million square kilometres. The continental shelf is relatively narrow in the north but widens progressively to the south, where it reaches a width of about 850 km. This ecosystem, a composite area with a unique combination of characteristics, is influenced by two major wind-driven currents: the northward flowing Malv- inas (Falkland) Islands Current and the southward flowing Fig. 1 Observations made with (grey crosses) and without (black Brazil Current (Bakun 1993). Of this complex oceanogra- diamond) mitigation measures. Grey shading represents all satellite monitoring records from the freezer trawlers fleet for the years 2008 phy, the area which extends from Argentina southward to and 2009. Isobaths: 50 m. (dotted line) and 200 m. (continuous line) Tierra del Fuego and eastward around the Malvinas (Falkland) Islands is probably the largest domain of its kind in the world (Croxall and Wood 2002). This environment cod (Salilota australis) (6216 mt) and rock cod provides fertile conditions for zooplankton production (Patagonotothen ramsayi) (12,398 mt). which is consumed by fish and squid that sustain substan- tial populations of seabirds, seals and whales (Croxall and Species and abundance of seabirds associated Wood 2002), but also several coastal and high seas trawl with the fishing vessels fisheries (Bertolotti et al. 2001; Sullivan et al. 2006b). The target fishery includes 33 stern factory trawlers that Seabird species and abundance of seabirds associated with operate year round over the Patagonian shelf between 41°S fishing vessels were estimated by conducting approxi- and 54°S (Fig. 1). Vessels are 67.8 ± 8.6 m total length mately 10-min counts from the stern gantry in a 250-m (range = 58–94.9 m) and use demersal trawl nets semicircular sampling area. This information was gathered (120–200 mm stretched mesh size at the cod end; *3.5–4 onboard during 218 censuses from 172 of 389 hauls (141 and 40–50 m vertical and horizontal aperture, respec- fishing days) from Spring (October–November 2008, 84 tively). Vessels trawl at a velocity of four knots, with trawl censuses), Winter (August–September 2009, 52 censuses), durations of between 3 and 4 h and trips that last between Summer (January–February 2010, 31 censuses) and Au- 30 and 60 days. The total catch per year between 2008 and tumn (May–June 2010, 51 censuses) by two experienced 2010 averaged 173,232 metric tonnes (mt), representing a seabird observers (authors LLT and LNC). In addition, a quarter of the total catch of all Argentine fisheries (Sań- range of environmental (Beaufort scale, cloud cover, wind chez et al. 2012). The main target species is the Argentine speed and relative wind direction) and operational vari- Hake (Merllucius hubbsi) with an average annual catch of ables (date, location and time) was also recorded. The 66,347 mt although, depending on market demand and censuses were made at least once per haul during trawling. hake quota during the year, vessels may change strategy to During all trips, seabirds associated with the vessel were target hoki (Macruronus magellanicus) (an annual average identified to species level. Frequency of occurrence was catch of 59,354 mt), kingklip (Genypterus blacodes) defined as the percentage of hauls in which each species (6666 mt), grenadier (Macrurus fasciatus) (6570 mt), red was observed.

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Seabird interactions two continuous covariates: relative wind speed and cloud cover. Sea state was not considered as this factor was found Information on net entanglements was obtained during the to correlate with season. The data collected in the 3 years haul for each of the 389 hauls, recording species, maturity of analysis were combined—within seasons and fishing and the number of birds caught. Data on interactions with areas—and analysed as if they were from 1 year to reduce trawl cables were collected for periods of 15–40 min, often the variance of the low sampling effort. including more than one observation period per haul. Data were collected simultaneously for both the starboard and Seabird mortality port warps but treated separately as discard was not expelled from both sides of the vessels in equal measure. Previous estimates of seabird mortality in trawl fisheries For each observation period, the following was recorded: have been based on records of corpses, or part thereof, mitigating measure (with/without); discard (none/low/ hauled on board (Sullivan et al. 2006b; Favero et al. 2011). medium/strong). For seabird collisions with trawl cables These estimates are likely to be an underestimate, because the following was recorded: species, maturity (adult/im- many birds become dislodged from the cable prior to mature), severity (heavy/medium/light, Table 1), approach hauling (Sullivan et al. 2006b). direction relative to the ship taking the bow as 0° (0°/90°/ The estimated number of seabirds killed by the factory 180°/270°) and outcome (dead/injured/drowned/unharmed, trawlers fleet was calculated by the number of collisions Table 1). Observations were conducted between daybreak with a known outcome for trawls conducted in the absence and twilight and throughout the area of fleet operation of mitigation measures. We assessed the distribution of (Fig. 1). data in two stages. The first stage was for collisions that resulted in mortality (subsequently referred to as dead) and Factors affecting seabird collision rate the second when collisions resulted in mortality or lethal injury (dead or injured). From the estimators (collision Generalised linear models were used to examine factors rate) we used the sum of bird collisions with a result of that might affect seabird collisions with trawl cables. The dead or injured divided by the sum of hours of observation number of collisions per hour of observation was used as (Cochran 1963; Bartle 1991; Hilborn and Mangel 1997; the response variable. The analyses were based on a neg- Thompson 2002; Favero et al. 2003): P ative binomial distribution, since this distribution is rec- bi ommended for count data with strong asymmetry to the B^ ¼ P H h right and in which the variance is greater than average i (Weimerskirch et al. 2000; Crawley 2007; Gonza´lez-Ze- B^ = Estimated total seabirds collisions, bi = Sum of sea- vallos et al. 2011). We only considered observations con- birds collisions, hi = Sum of hours of observation, ducted in the absence of mitigation measures and also h = Total of hours of trawl in the fishery. discarded observations in coastal areas because they do not As the distribution was found to differ from a normal represent traditional fishing grounds for the study fleet distribution, confidence intervals were calculated using a (n = 34). nonparametric bootstrap (Crawley 2007). For each fre- We conducted a stepwise procedure (Weimerskirch quency table (dead and dead or injured), count data were et al. 2000; Crawley 2007), and the following factors were re-sampled with replacement per observation and proposed evaluated in this analysis: season (4 levels), time of day (4 estimators calculated for each new data set. The estimator levels, 8–11 am MA, 11 am–2 pm ME, 14–18 pm MT, confidence intervals were constructed from the 0.05 and 18–20 pm TN), direction of approach relative to the vessel 0.95 quartiles of all estimators obtained in the simulation. (4 levels), and discard (4 levels). The model also included Total fishing effort (days) were obtained from vessel

Table 1 Type of impacts Variable Categories Deﬁnition describing the interaction between seabirds and ﬁshing Severity Heavy Impact that shakes or drags under water the bird gear Medium Impact that causes change in behaviour and direction Light Touch that causes little or no change in behaviour or direction Outcome Dead Bird visible dead on water or cable Injured Bird generally with broken wings Drowned Bird drags under water Unharmed No visible damage

123 Polar Biol monitoring system data and used to extrapolate observed paced every 2.5 m. Buoys with 1.8 kg weights or a spe- data to fleet level. The total fishing effort in days was cially designed off-setting towed device to prevent the available for the years 2008 and 2009, and we calculated an entanglement between cables and BSLs (called Tamini average of the 2 years to obtain a single value (Table 2). Tabla, ACAP 2013b) were fixed at the terminal end to To convert fishing effort from fishing days to fishing hours, create drag and maximise their aerial extent. A Wilcoxon– we used information from 1000 trawls based on data pro- Mann–Whitney test was used to compare observed colli- vided by the National Observer Programme of the Instituto sions between seabirds and cables with and without BSLs Nacional de Investigacioń y Desarrollo Pesquero (INI- deployed. There were no significant differences between DEP). Trawl duration was defined as the time from when collisions observed with a BSL deployed when using a nets reached operational trawl depth to the moment win- buoy or the towed device (Test Wilcoxon–Mann–Whitney, ches started hauling. p = 0.1891), so data from both treatments were pooled. All The observed trawl duration from INIDEP data was statistical analyses were performed using R software assessed by season, and significant differences were found v2.13.0 (R Development Core Team 2006). between seasons (ANOVA of mean trawl duration for seasons, p \ 0.0001). Therefore, the number of fishing days per season was converted to the number of fishing Results hours per day according to season (Table 2). An annual mortality estimate was calculated for each Observer coverage species (without seasonal stratification) based on estimated fishing effort (the sum of hours from each season), the Between October 2008 and June 2010, we observed four hours of observation effort and number of collisions that cruises, one per season, on two different factory trawlers. resulted in death or injury. The estimator used was the sum This represented 141 days and 389 trawls, with 146.5 h of of bird collisions divided by the sum of hours observed as direct observation of trawl cables. For logistical reasons, according to Hilborn and Mangel (1997) and Bartle (1991), data analysis was based on observations of these two and this better represents the asymmetrical grouping of vessels. However, the vessel selection process was not data. Confidence intervals were calculated for each rate related to factors that are known or thought to influence using resampling techniques. seabird mortality. The observation effort covered the main areas of the fleet (Fig. 1), and therefore, an unbiased ran- Mitigation measures dom sample was assumed for the study fleet (Klaer and Polacheck 1995; Polacheck and Klaer 1997). As a mitigation measure, bird-scaring lines (BSLs, Fig. 2) A total of 482 observation periods directly monitoring were deployed from port and starboard sides of the vessel, the trawl cables were conducted over 146.5 h, of which attached 2 m above and outside the blocks so as to main- 53.6 h were with mitigation measures deployed and 92.9 h tain a minimum aerial extent of 20 m. Although the vessels in the absence of mitigation. Our observation effort of had more discharge on one side (typically the port side), 92.9 h in the absence of mitigation was equivalent to the effectiveness of the BSLs was assessed on both port between 0.053 and 0.394 % of total fleet effort, depending and starboard sides. Each BSL consisted of 30 m of 10-mm on the season (Table 2). The factors affecting seabird green and yellow polypropylene line with streamers of collisions with trawl cables and seabird mortality estimates branched, brightly coloured, UV protected, red ribbon presented here were based on observations conducted in

Table 2 Fishing days obtained from satellite monitoring for the years 2008 and 2009 and average hours of ﬁshing effort per day obtained from INIDEP National Observer Programe records Season Fishing days 2008–2009 Average Hours ﬁshing effort per day Total hours Hours observed % Coverage 2008 2009

Summer 1622 1404 1513 13.34 20,181 10.60 0.053 Autumn 1532 1315 1424 8.67 12,341 13.00 0.105 Winter 1285 1151 1218 8.64 10,518 13.48 0.128 Spring 1559 1111 1335 10.60 14,149 55.78 0.394 Hours observed hours of observation effort monitoring trawl warp cables without mitigation measures, % coverage percentage coverage based on the estimated total number of hours ﬁshing effort

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Fig. 2 Diagram of bird-scaring lines (BSLs) used at freezer trawlers showing the warp cables and the lines components

full daylight in the absence of mitigation measures, which From observation of collisions with trawl cables, a total mirrors the current situation in the industrial trawl fleet. of 36 black-browed albatross corpses were hauled aboard, resulting in a mortality rate of 0.093 birds/haul with a mean Seabird species and abundance haul duration of 3.9 h. Mean haul duration was calculated using national observer data (SD = 1.49 h, n = 988 In total, 17 species of seabird were recorded foraging on hauls). No seasonal differences were observed (Table 5). discards aft of factory trawlers (Table 3). The most fre- From direct observation, we recorded 3115 seabird quent species were black-browed albatross Thalassarche collisions with trawl cables split into 733 heavy, 1154 melanophris and southern giant petrel Macronectes medium and 1228 light impacts (see Table 1). The giganteus, followed by the southern royal albatross Dio- majority of collisions with trawl cables in the industrial medea epomophora, Cape petrel Daption capense, and trawl fleet were from Cape petrel (1355 collisions recor- white-chinned petrel Procellaria aequinoctialis. The rest of ded); black-browed albatross (1350); southern giant petrel the species were observed in low numbers and in\50 % of (281); northern giant petrel (71) and white-chinned petrel hauls (Table 3). The abundance of seven of the eight sea- (37). There were ten or less collisions of the following bird species most frequently associated with this fishery species: great shearwater Puffinus gravis, kelp gull Larus (black-browed albatross, southern giant petrel, northern dominicanus, sooty shearwater, southern royal albatross giant petrel, Cape petrel, Wilson´s storm petrel Oceanites and Wilson’s storm petrel. The collisions were recorded oceanicus, southern royal albatross, white-chinned petrel mainly on the Patagonian Shelf, except for the kelp gull and sooty shearwater Puffinus griseus) varied amongst and great shearwater which occurred off the coast in the seasons (Table 4). In general, abundances were higher in Santa Cruz province. Of the collisions recorded for black- winter and autumn with the exception of Wilson’s storm browed albatrosses, 12 % corresponded to juveniles. petrel, which was greater in spring and the southern giant These observations give a total collision rate of 33.53 petrel, which remained constant through all seasons birds/h, calculated as the sum of all interactions (regardless (Table 4). of impact level or outcome) divided by the sum of obser- During most hauls, between one hundred and five vation effort. Considering the different kinds of impacts, thousand seabirds actively surrounded the net as it reached the collision rate was: 0.15 birds/h for dead birds and 0.33 the surface and until the cod end was retrieved. It was birds/h for dead plus injured for all species together. impossible to quantify these interactions due to the high numbers of seabirds. Factors affecting the collision rate in the absence of mitigation measures Seabird interactions Statistical analyses of the factors affecting the collision rate Despite the large numbers of seabirds around the fishing in the absence of mitigation measures focused on all spe- nets and probably because of the relatively small mesh size cies of seabirds and those which showed a greater inter- of demersal trawl nets, there were only six (0.013 birds/ action with the study fleet: black-browed albatross, haul) black-browed albatross mortality records due to net southern and northern giant petrels, Cape petrel, and white- entanglement during the haul (n = 389 hauls). No seasonal chinned petrel. The factor that affected all bird species in differences were observed (Table 5). the absence of mitigation measures was the direction of

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Table 3 Frequency of Species Frequency of occurence Mean (range) occurrence (%) and mean numbers (range in parentheses) Black-browed albatross 97.1 387.8 (0–1800) per haul of seabirds attending factory trawlers on the Thalassarche melanophris Patagonian Shelf during Southern giant petrel 89.5 96.7 (0–540) 2008–2010 Macronectes giganteus Southern royal albatross 83.7 7.5 (0–80) Diomedea epomophora Cape petrel 82.0 294.3 (0–1700) Daption capense White-chinned petrel 51.2 17.2 (0–340) Procellaria aequinoctialis Northern giant petrel 35.5 28.7 (0–300) Macronectes halli Wilson´s storm petrel 26.2 20.0 (0–280) Oceanites oceanicus Sooty shearwater 21.5 4.8 (0–340) Pufﬁnus griseus Kelp gull 20.3 2.5 (0–84) Larus dominicanus Slender-brilled prion 7.0 0.7 (0–51) Pachyptila belcheri Great shearwater 5.8 0.2 (0–10) Pufﬁnus gravis Southern fulmar 4.1 0.2 (0–13) Fulmarus glacialoides Brown skua 3.5 0.2 (0–21) Stercorarius antarticus Grey-headed albatross 2.3 0.02 (0–1) Thalassarche chrysostoma Royal northern albatross 2.3 0.05 (0–3) Diomedea sanfordi South American tern 1.2 0.1 (0–12) Sterna hirundinacea Wandering albatross 0.6 0.01 (0–2) Diomedea exulans

approach relative to the vessel (p \ 0.0001, Table 6) and Seabird mortality estimate and mitigation measures season affected black-browed albatross, Cape petrel and southern giant petrel. Time of day affected black-browed Our estimates of seabirds mortality, developed from albatross, northern giant petrel and white-chinned petrel. information collected in the absence of BSLs and using Discard rate was a significant factor for only the most pooled fishery effort data from 2008 to 2009, suggest frequently observed species, black-browed albatross and 13,548 (CI 8000–19,673) black-browed albatrosses; 2463 Cape petrel. Finally, cloud cover only affected southern (CI 612–4306) southern giant petrels; 1847 (CI 61–689) giant petrel (Table 6). All models were explained by northern giant petrels and 1232 (CI 0–3077) Cape petrels greater than 65 % of deviation and presented a good fit are killed or injured per year (Table 7). (comparison of residual deviation vs. degrees of freedom; Mitigation measures caused significant differences in Crawley 2007). The observer and boat effect could not be the collision rate of all seabirds with trawl cables when estimated because the sample size was too small to enable comparing results from observations with and without these analyses. BSLs (Mann–Whitney Wilcoxon test: p \ 0.05).

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Table 4 Mean (range in parentheses) abundances per haul for the eight most abundant seabirds attending factory trawlers on the Patagonian Shelf during 2008–2010 Summer Autumn Winter Spring Kruskal–Wallis (n = 31) (n = 51) (n = 52) (n = 84) H p

Black-browed albatross 264.7 (0–1250) 508.8 (0–1800) 529.1 (30–1700) 272.3 (0–1120) 21.978 \0.001 Southern giant petrel 83.4 (0–450) 73.5 (0–400) 100.0 (13–400) 113.5 (0–540) 6.336 0.096 Southern royal albatross 4.3 (0–16) 9.5 (0–30) 11.5 (0–80) 5.0 (0–27) 23.29 \0.001 Cape petrel 0.3 (0–10) 258.8 (0–900) 640.7 (20–1700) 210.0 (0–980) 106.952 \0.001 White-chinned petrel 31.0 (0–105) 9.7 (0–340) 6.4 (0–92) 23.5 (0–280) 49.818 \0.001 Northern giant petrel 16.9 (0–180) 32.6 (0–250) 76.4 (0–300) 1.1 (0–30) 97.075 \0.001 Wilson’s storm petrel 1.1 (0–15) – 0.04 (0–2) 51.6 (0–280) 105.720 \0.001 Sooty shearwater 0.9 (0–10) – 17.1(0–340) 1.7 (0–26) 42.203 \0.001 Mean of birds per haul 442.6 (15–1527) 1010.4 (65–2860) 1406.2 (137–3847) 799.3 (14–2161) Total species 12 10 12 10

Table 5 Black-browed Entanglement Summer Autumn Winter Spring Total Rate Kruskal–Wallis albatrosses hauled aboard killed during 389 hauls in factory (n = 80) (n = 91) (n = 111) (n = 107) (n = 389) bird/haul Hp trawl vessels on the Patagonian Shelf during 2008–2010 Net 1 1 3 1 6 0.013 0.002 0.9955 Warp cable 6 8 15 7 36 0.093 0.99 0.1274

Table 6 Results of generalised Factors Species linear models for all seabirds and for the ﬁve most abundant All BBA SGP NGP CP WCP

Relative wind direction ??? Cloud cover ??? Discard rate ??? ??? ??? Direction of approach relative to the vessel ??? ??? ??? ??? ??? ??? Time of day ?? ? ? ? Season ??? ??? ??? ??? Model with significant factors Residual deviation 229.79 170.56 77.60 25.81 184.00 14.79 Degrees of freedom 238 205 147 99 194 87 % of deviation explained 76 81 87 95 65 94 BBA Black-browed albatross, SGP southern giant petrel, NGP northern giant petrel, CP cape petrel, WCP white-chinned petrel Significance level is indicated by the symbol number. ? (p \ 0.01): low, ?? (p \ 0.001): medium, ??? (p \ 0.0001): highly significant

Performing the analysis by species (considering only the specifically designed towed device (p = 0.1891). It was main species that collide with trawl cables according to the only possible to repeat the analysis for black-browed present study) also gave significant differences between albatross, and no significant differences in collision rate observations with and without BSLs (Table 8). This anal- were found when using the different towed devices ysis does not address the level of impact or outcome, only (p = 0.3014). As low numbers of collisions were recorded collisions per hour. in both mitigation treatments, it is likely that the number of There were no significant differences between collisions zero values hinders the comparison between the two observed with a BSL deployed when using a buoy or a observations (Table 9).

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Discussion fisheries in the area (Sullivan et al. 2006b; Favero et al. 2011). However, the species composition differs from that Seabird assemblage reported for coastal trawl fisheries in the same region where the kelp gull featured as the dominant species Seventeen seabird species scavenged on fishery discards (registered in 34 coastal hauls in our study) plus pursuit from the Hake industrial trawl fishery on the Patagonian diving species such as the imperial shag (Phalacrocorax Shelf. Some species were present in the majority of trawls, atriceps) and Magellanic penguin (Spheniscus magellani- while others were recorded infrequently or in low numbers. cus) attending the vessels (Gonza´lez-Zevallos and Yorio Flocks of between ten birds and five thousand birds 2006; Marinao and Yorio 2011). attended the vessels, with black-browed albatross, southern The species recorded attending the factory trawlers giant petrel and Cape petrel dominating the assemblages included breeding birds from along the coast of Patagonia, and southern royal albatross and white-chinned petrel Malvinas (Falkland) Islands, South Georgia and Antarctica. present in lower numbers, a similar situation to other trawl Others from more remote sites such as islands around New Zealand represent non-breeders visiting the rich Patagonian Continental Shelf to forage (Croxall and Wood 2002). Table 7 Rates, estimation and confident intervals of birds dead or Some 41 % of the recorded species (including all the injured by the result of colliding against the warp cables albatross) are considered threatened (Near threatened, Species Number of collisions Vulnerable or Endangered categories) according to the Dead Dead ? injured IUCN Red List (BirdLife International 2014a), highlighting the importance for observer programmes to record the BBA 12 22 interactions between seabirds and this fishery. SGP 0 4 Black-browed albatross were recorded attending vessels NGP 0 3 year round with peak abundance in autumn and winter. CP 2 0 This contrasts the situation in the nearby waters of the Birds/hour Malvinas (Falkland) Islands, probably because birds return BBA 0.129 (0.097–0.205) 0.237 (0.140–0.304) to breeding grounds around the islands and forage locally SGP 0 0.043 (0.011–0.075) for a large part of the breeding season (White et al. 2002). NGP 0 0.032 (0.011–0.065) However, black-browed albatross, giant petrels and Cape CP 0.022 (0–0.054) 0 petrel attended the vessels in both our study area and the Estimate Malvinas (Falkland) Islands in huge numbers (Sullivan BBA 7390 (5536–11,695) 13,548 (8001–19,673) et al. 2006b). The mean abundance of black-browed alba- SGP 0 2463 (612–4306) tross and other species is lower (in some cases by an order NGP 0 1847 (612–3689) of magnitude) in trawl fisheries where the fish catch is CP 1232 (0–3077) 0 stored on ice (ice-trawlers). The main factor that explains Bold values indicate main results for black-browed albatross this difference is that only whole fish and invertebrates are Birds/hour: sum of the birds colliding per sum of observations. Esti- discarded from ice-trawlers (Gonza´lez-Zevallos and Yorio mate: Rate 9 fishing effort. Total hours: 57,188; Observed hours: 92.9 2006; Favero et al. 2011; Marinao and Yorio 2011). The BBA Black-browed albatross, CP cape petrel, NGP northern giant presence of offal in the discharge is a major factor affecting petrel, SGP southern giant petrel seabird numbers around trawlers (Weimerskirch et al.

Table 8 Comparison between Species With BSL Without BSL W p observations with and without a bird-scaring line (BSL) Obs. Birds/hour Obs. Birds/hour deployed BBA 204 2.63 228 16.97 36,668 \0.001 SGP 185 0.17 162 5.07 22,272 \0.001 NGP 179 0 109 1.88 12,441 \0.001 CP 201 1.49 206 18.63 31,835 \0.001 WCP 179 0 99 1.07 10,650 \0.001 All species 217 4.01 264 33.59 45,312 \0.001 Obs. number of observations, Birds/hour sum of the birds colliding per sum of hours of observation, W Mann–Whitney–Wilcoxon test, ppvalue. BBA black-browed albatross, SGP southern giant petrel, NGP northern giant petrel, CP Cape petrel, WCP white-chinned petrel

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Table 9 Comparison of Species Buoy TT W p observations between bird- scaring lines with two different Obs. Bird/h Obs. Bird/h towed devices: buoy and Tamini Tabla (TT) Black-browed Albatross 99 1.327 98 1.011 5099.5 0.2833 All 107 1.787 103 1.425 5900 0.1879 Obs. number of observations, Birds/hs sum of the birds colliding per sum of hours of observation, W Mann– Whitney–Wilcoxon test, ppvalue

2000) as well as fishing areas, discard volumes and con- Modelling the seabird behaviour, plus environmental dition (e.g. Abraham et al. 2009). and operational factors affecting the collision rates for all species indicated a clear significance for discard rate, Seabird interactions season and direction of approach relative to the vessel. The effects of discard in the collision rates is a well-known Interactions between seabirds and pelagic and bottom phenomenon and has been recorded by several studies of trawlers in the south-west Atlantic are well known, espe- trawl fisheries (Gonza´lez-Zevallos and Yorio 2006; Sulli- cially for three parts of the fishing gear: the net, trawl van et al. 2006b; Watkins et al. 2008; Favero et al. 2011). cables and net sonde cable (Tamini et al. 2002; Gonza´lez- According to our results, the abundance of seabirds—and Zevallos and Yorio 2006; Sullivan et al. 2006b; Gonza´lez- hence the number of collisions—were very low during the Zevallos et al. 2007; Favero et al. 2011; Marinao and Yorio first haul of the day which was associated with zero dis- 2011; BirdLife International Marine Programme 2014). cards. The variable season—closely liked of sea state— The trawl cables are a major threat for species of the order which is often linked to swell height was found to be Procellariiformes which frequently forage behind the ves- significant in other similar studies Sullivan et al. (2006b). sel with open wings. As a result of these strikes, birds are The most important factor was direction of approach rel- often trapped and forced underwater by the drag created by ative to the vessel, which was true for all species plus each the forward motion of the fishing vessel (Sullivan and Reid species separately. 2002; Gonza´lez-Zevallos and Yorio 2006). The strike rates observed in trawler fleets are associated with a wide Significance of seabird mortality rates spectrum of factors including vessel size and type, capture volume, fishing areas, seabird assemblages, type and Like all at-sea data collection, estimating seabird mortality amount of discharge amongst others (Favero et al. 2011). caused by cable strike has several challenges that should be In this study we observed a rate of 33.50 collisions per hour addressed to ensure representative and reliable data: (1) for all species, which is similar to the value found for ice- placement of an appropriate level of observer coverage in trawlers (25.47 per hour, Favero et al. 2011), and lower space and time is expensive, and often not feasible (2) than that for factory trawlers operating in neighbouring ensuring that observers have specific protocols to record areas (55.78 per hour, Sullivan et al. 2006a). However, the trawl cables impacts for extended periods of time (in some rate observed by Sullivan et al. (2006a), corresponded to a cases[10 h trawling/day) and, (3) obtaining access to fleet trip between August and November when albatross density fishing effort data in an appropriate format (hauls or hours and incidental capture peak around fishing vessels in of trawl) can be a politically difficult task (Moore and Malvinas (Falkland) Island waters (Sullivan et al. 2006b). Zˇ ydelis 2008). Beyond the strike rate, an important difference between As in Watkins et al. (2008), we recognise our extrapo- ice-trawlers and factory trawlers is in the rate of heavy lated mortality estimates are based on a relatively low level impacts. Our results indicate a rate of 8.36 collisions/hour of observer coverage (0.05–0.39 % per season) and as such against 16.80 for other factory trawler fleets in the area should be interpreted with caution, but the potential scale (Sullivan et al. 2006a) and 0.04 for ice-trawlers (Favero of seabird mortality in this fleet is a significant concern. et al. 2011). Moreover, several authors found a positive Even if mortality lies at the lower end of the CI, it suggests correlation between heavy contacts and mortality (Sullivan that at least 9200 seabirds are killed each year, including et al. 2006b; Maree et al. 2014). While mortality is a sta- 8000 black-browed albatross. Several studies in freezer tistically rare event, and it is difficult to obtain a sufficient trawl fisheries have offered similar results with high mor- sample size for analysis, heavy impacts can be used as an tality of this species. It represents the predominant species index of mortality, although the correlation requires vali- killed during the 2002–2003 season in the Malvinas dation for each new area and fishery studied (Sullivan et al. (Falklands) Island (Sullivan et al. 2006b) and during 2006b). 2004–2005 in South African waters together with Shy

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Albatross Thalassarche cauta (Watkins et al. 2008). made the adoption of mitigation measures more acceptable Additionally, a study using remote sensing techniques to for the crew of the vessels, especially in adverse weather model the degree of spatial overlap between black-browed conditions. albatross and both longline and trawl fisheries in the This study represents the first estimate of seabird mor- Patagonian Shelf indicated very high spatial and temporal tality caused by the Argentine stern factory trawl fishery and overlap between 35 and 38°S and 45 and 47°S during the proposes simple and economic solutions to reduce the winter (Copello et al. 2014). However, this species has impact. Although a larger data set could improve the model, been downlisted recently to near threatened (from Endan- the considerable impact of the fishery on seabirds is unde- gered in the IUCN categories) as it is no longer estimated niable, especially the black-browed albatross, a species that to be undergoing rapid population declines but still suffers is affected by several others fisheries in the Atlantic Ocean. high levels of mortality in longline and trawl fisheries in Since 2010, Argentina has adopted the National Plan of the South Atlantic (BirdLife International 2014b). Action–Seabirds (NPOA-S), the main objective of which is to reduce the interaction between seabirds and fisheries in Mitigation measures waters under Argentinean jurisdiction. However, the implementation of mandatory measures for reduce the Of the mitigation measures available to reduce seabird seabirds bycatch was only applied to longline fisheries, a collisions against trawl cables and hence the trawler-asso- fleet that currently includes three vessels compared with ciated seabird mortality—bird-scaring lines, warp scarers, *170 industrial trawlers. Our study concurs with others the Brady bafflers, traffic cones amongst others—the bird- highlighting the need for the urgent adoption of mitigation scaring lines have the advantage of low cost, requiring little measures for this fleet. storage space and easy to maintain, replace and deploy (Maree et al. 2014). Possible problems associated with Acknowledgments Thanks to those who provided the necessary BSLs include: (1) mortalities may occur before the device and indispensable data for this study. Gabriela Navarro and Gustavo Martinez of the Direccioń Nacional de Planificacioń Pesquera, is deployed during shooting and after it is retrieved before Subsecretarıá de Pesca y Acuicultura de la Nacioń and Gabriel hauling (Sullivan et al. 2004) and (2) unpredictable beha- Blanco of the National Observer Programe, Instituto Nacional de viour of the BSL streamers and potential entanglement Investigacioń y Desarrollo Pesquero (INIDEP). The Albatross Task with the trawl cables. Force is funded through The Royal Society for the Protection of Birds and BirdLife International. Special thanks to the company Pescargen The adaptation of the BSLs—from longliners to traw- S. A. and the captains and crews of the Pescargen IV and V. lers—included three different aspects: materials, configuration and point of attachment to the vessels. Common materials used in trawlers are ropes for the backbone and References hoses or plastic strips for the streamers (Sullivan et al. 2006a). The main characteristics of the configuration are Abraham ER, Pierre JP, Middleton DAJ, Cleal J, Walker NA, Waugh the length of the backbone—between 30 and 50 m—and SM (2009) Effectiveness of fish waste management strategies in the distance between streamers—2,5 to 5 m—while the reducing seabird attendance at a trawl vessel. Fish Res 95:210–219. doi:10.1016/j.fishres.2008.08.014 length of the streamers should always reach the sea surface ACAP (2013a) ACAP Summary advice for reducing impact of in calm conditions (Sullivan et al. 2006a). The attachment demersal longlines on seabirds. http://www.acap.aq/index.php/ point of the backbone is 2 m outboard of either trawl cable. en/bycatch-mitigation/cat_view/128-english/392-bycatch-mitiga Our results suggest the configuration of a 30 m backbone tion/391-mitigation-advice ACAP (2013b) Tasa de mortalidad de aves marinas y pruebas de and red plastic streamers placed every 2.5 m reduced the eficiencia de lıńeas espantapa´jaros en la flota congeladora de amount of impacts significantly (Fig. 2). The main differ- arrastre de fondo del Mar Argentino. La Rochelle, Francia ence between our work and previous studies is the distance Anderson ORJ, Small CJ, Croxall JP, Dunn EK, Sullivan BJ, Yates O, between streamers (2.5 vs. 5 m). We decided to adjust this Black A (2011) Global seabird bycatch in longline fisheries. End Species Res 14:91–106 having initially observed some black-browed albatross Bakun A (1993) The California Current, Benguela Current, and passing though streamers that were separated by 5 m Southwestern Atlantic Shelf ecosystems; a comparative (Tamini, personal observation). Finally, two towed devices approach to identifying factors regulating biomass yields. In: were used in this study: a buoy and the Tamini Tabla Sherman K, Alexander DG, Gold BD (eds) Large marine ecosystems: stress mitigation, and sustainability. AAAS Press, (ACAP 2013b). We found no significant differences Washington. p 199–221 between impacts of black-browed albatross with trawl Bartle JA (1991) Incidental capture of seabirds in the New Zealand cables when comparing these towed devices as BSLs were subantarctic squid trawl fishery. Bird Conserv Int 1:351–359 highly effective in both cases. However, the Tamini Tabla Bertolotti MI, Hernańdez DR, Pagani AN, Castan˜eda MF (2001) Estratificacioń y estimacioń de los rendimientos de la flota de device reduced entanglements between the BSLs and the buques procesadores congeladores arrastreros. El Mar Argentino trawl cables (Tamini, personal observation) and therefore y sus Recursos Pesqueros 3:71–88 123 Polar Biol

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