Elsevier

Biological Conservation

Volume 205, January 2017, Pages 60-76
Biological Conservation

Review
Global patterns of sex- and age-specific variation in seabird bycatch

https://doi.org/10.1016/j.biocon.2016.11.028Get rights and content

Highlights

  • We reviewed 44 studies reporting sex and age composition of seabird bycatch.

  • Bycatch was highly biased by sex (65% of 123 samples) and age (92% of 114 samples).

  • Sex- and age-biases in bycatch were mainly related to differential at-sea distributions.

  • Population impacts of bycatch are exacerbated by sex- and age-biased mortality.

  • Recording of seabird sex and age should be routine in bycatch observer programs.

Abstract

Fisheries bycatch is a major threat to seabird populations, and understanding sex- and age-biases in bycatch rates is important for assessing population-level impacts. We analysed 44 studies to provide the first global assessment of seabird bycatch by sex and age, and used generalised models to investigate the effects of region and fishing method. Bycatch was highly biased by sex (65% of 123 samples) and age (92% of 114 samples), with the majority of samples skewed towards males and adults. Bycatch of adults and males was higher in subpolar regions, whereas there was a tendency for more immatures and females to be killed in subtropical waters. Fishing method influenced sex- and age-ratios only in subpolar regions. Sex- and age-biases are therefore common features of seabird bycatch in global fisheries that appear to be associated largely with differences in at-sea distributions. This unbalanced mortality influences the extent to which populations are impacted by fisheries, which is a key consideration for at-risk species. We recommend that researchers track individuals of different sex and age classes to improve knowledge of their distribution, relative overlap with vessels, and hence susceptibility to bycatch. This information should then be incorporated in ecological risk assessments of effects of fisheries on vulnerable species. Additionally, data on sex, age and provenance of bycaught birds should be collected by fisheries observers in order to identify regions and fleets where bycatch is more likely to result in population-level impacts, and to improve targeting of bycatch mitigation and monitoring of compliance.

Introduction

Fisheries are one of the primary threats to marine biodiversity, impacting ecosystems from the open ocean to the coast, and from the poles to the tropics (Halpern et al., 2008, Jackson et al., 2001). Commercial fishing has resulted in severe and widespread ecosystem disruption primarily as a result of over-harvesting, habitat degradation and the mortality of non-target species, also called bycatch (Hall et al., 2000, Halpern et al., 2008, Jackson et al., 2001). Populations of large marine vertebrates, such as sea turtles, sharks, marine mammals, and seabirds, are particularly susceptible to bycatch because of a combination of their attraction to fishery bait and discards, and their naturally slow reproductive rates rendering them sensitive to even small increases in mortality (Hall et al., 2000, Lewison et al., 2004). The impacts are so extensive that the recent declines of many large marine vertebrates resulting from bycatch have been compared to the historical extirpations and extinctions of terrestrial megafauna by human hunting (Lewison et al., 2004, Lewison et al., 2014).

Seabirds are particularly at risk from fisheries, as they are bycaught in a wide range of gear types (Croxall et al., 2012, Montevecchi, 2002, Phillips et al., 2016). For example, drift nets set by Japanese, Korean and Taiwanese vessels are estimated to have killed up to 40 million sooty (Ardenna grisea) and short-tailed (A. tenuirostris) shearwaters in the North Pacific between 1952 and 2001 (Uhlmann et al., 2005). Coastal gillnet fisheries are also a major source of mortality, with > 400,000 seabirds killed annually, worldwide (Žydelis et al., 2013). Global longline fisheries are estimated to have killed at least 160,000, and potentially 320,000 seabirds annually, mainly albatrosses, petrels and shearwaters (Anderson et al., 2011). Trawl fisheries are also a threat, with about 9300 birds, mostly albatrosses, estimated to be killed annually just in the waters off South Africa by wet fish trawls (Maree et al., 2014, Sullivan et al., 2006, Waugh et al., 2008). These levels of mortality have led to severe declines in many populations and are clearly unsustainable (Croxall et al., 1998, Cuthbert et al., 2005, Delord et al., 2008, Phillips et al., 2016, Piatt and Gould, 1994, Rolland et al., 2010, Žydelis et al., 2009, Žydelis et al., 2013).

The impact of bycatch depends not only on the number of individuals killed, but also on the components of the population that are impacted (Bugoni et al., 2011, Lewison et al., 2012). For example, because seabird life histories are characterized by delayed maturation, high survival and low rates of reproduction, mortality of adults will have greater population-level impacts than mortality of immatures (Lewison et al., 2014). Moreover, because seabirds are monogamous, with obligate biparental care, sex-biased mortality in fisheries can reduce the effective population size (Mills and Ryan, 2005, Weimerskirch et al., 2005). Sex- and age-biases in seabird bycatch are reported in a number of fisheries (Awkerman et al., 2006, Gales et al., 1998, Ryan and Boix-Hinzen, 1999, Stempniewicz, 1994), and there has been a review of adult sex-ratios (ASR) in bycatch of albatrosses and petrels (Bugoni et al., 2011). However, there has been no comprehensive review of sex- and age-biases in bycatch of seabirds in general, even though a better understanding of their nature and extent is required to determine the full impact of bycatch on populations and communities. Indeed, this has been identified as one of the highest priority research questions in the field of seabird ecology and conservation (Lewison et al., 2012, Phillips et al., 2016).

Accordingly, the aim of the current study is to provide the first global review of age- and sex-specific bycatch in seabirds. This will contribute towards a better understanding of the frequency and magnitude of these effects across taxa, regions and fishery gear-type, as well as the implications for management and conservation. We predict that larger and more dominant individuals, usually adult males, will have higher bycatch rates than adult females, or younger birds of either sex, because they are better able to compete for discards and baits while attending fishing boats (Awkerman et al., 2007b, Bregnballe and Frederiksen, 2006, Croxall and Prince, 1990, Montevecchi, 2002). However, bycatch rates will also be influenced by region. Many studies have shown that females and immatures tend to travel further from their breeding sites, or to lower latitudes, compared with males and adults (Hedd et al., 2014, Phillips et al., 2004, Phillips et al., 2005). Therefore, because the majority of seabirds breed at high latitudes (Schreiber and Burger, 2002) we broadly predict that bycatch in subpolar (sub-Arctic and sub-Antarctic) areas will tend to be skewed towards males and adults, whereas in subtropical regions, bycatch will be biased towards females and immatures.

Section snippets

Literature review

We reviewed the literature for studies reporting sex and age composition of seabird bycatch in fisheries from around the world. We searched Thomson Reuters Web of Science and Google Scholar using the following search terms: topic = (seabird* OR albatross* OR petrel* OR penguin* OR shearwater*) and (sex OR age OR female OR male OR adult OR juvenile) and (fishery* OR bycatch OR mortality) and (bias); timespan = all years. To ensure the best possible coverage of the bycatch literature, we supplemented

Results

We found 44 studies, published between 1990 and 2016, that reported sex and age composition of seabird bycatch in fisheries, of which 35 (79%) were in the southern hemisphere and 9 (21%) in the northern hemisphere (Fig. 1, Table 1). Data were available from four main types of fishery: 14 studies for pelagic longline (32%), nine for demersal longline (20%), nine for gillnet (20%), two for trawl (5%). Seven (16%) studies reported data for more than one fishery, separated according to gear type.

Discussion

Sex- and age-biases in seabird bycatch have been reported in a number of fisheries (Delord et al., 2005, Gales et al., 1998, Nel et al., 2002a, Phillips et al., 2010, Ryan and Boix-Hinzen, 1999), and there is growing interest in both the underlying mechanisms and the potential demographic consequences (Bugoni et al., 2011, Lewison et al., 2012). Here we provide the first global synthesis of both sex and age-specific variation in seabird bycatch rates by different fisheries and in diverse

Conclusion

Sex and age biases in seabird bycatch are common features across global fisheries, mainly related to differential at-sea distributions. Overall, bycatch of adults and males was higher in subpolar regions and closer to colonies, whereas immatures and females were caught more frequently in subtropical waters. We found no compelling evidence that differences in sex and age ratios are related to the competitive advantage of males and adults foraging at fishing vessels, or to naivety of young birds

Acknowledgments

We thank Stuart Bearhop for providing constructive comments on the manuscript, and Hanna Nevins and Peter Ryan for providing valuable literature. We also thank Fabio Olmos for providing pictures of some of the birds composing our figures, and the three anonymous referees for their helpfull suggestions for improvements to the paper. This work is part funded via a scholarship to DG from the Sciences Without Borders Program (CNPq/Brazil, Proc. 246619/2012-0). The study represents a contribution to

References (121)

  • M.A. Hall et al.

    By-catch: problems and solutions

    Mar. Pollut. Bull.

    (2000)
  • R.L. Lewison et al.

    Understanding impacts of fisheries bycatch on marine megafauna

    Trends Ecol. Evol.

    (2004)
  • R.A. Phillips et al.

    Year-round distribution of white-chinned petrels from South Georgia: relationships with oceanography and fisheries

    Biol. Conserv.

    (2006)
  • R.A. Phillips et al.

    The conservation status and priorities for albatrosses and large petrels

    Biol. Conserv.

    (2016)
  • J.P. Seco-Pon et al.

    Effect of longline configuration on seabird mortality in the Argentine semi-pelagic kingclip Genypterus blacodes fishery

    Fish. Res.

    (2007)
  • B. Sullivan et al.

    Seabird mortality on factory trawlers in the Falkland Islands and beyond

    Biol. Conserv.

    (2006)
  • C.L. Abbott et al.

    Molecular provenance analysis for shy and white-capped albatrosses killed by fisheries interactions in Australia, New Zealand, and South Africa

    Conserv. Genet.

    (2006)
  • C.L. Abbott et al.

    Genetic structure of rhinoceros auklets, Cerorhinca monocerata, breeding in British Columbia, Alaska and Japan

    Mar. Biol.

    (2014)
  • ACAP - Agreement on the Conservation of Albatrosses and Petrels

    ACAP Species assessment: Campbell Albatross Thalassarche impavida

    (2009)
  • ACAP - Agreement on the Conservation of Albatrosses and Petrels

    ACAP Species assessment: Black-browed Albatross Thalassarche melanophris

    (2010)
  • ACAP - Agreement on the Conservation of Albatrosses and Petrels

    ACAP Species assessment: Grey-headed Albatross Thalassarche chrysostoma

    (2010)
  • D.J. Anderson et al.

    Non-breeding Nazca boobies (Sula granti) show social and sexual interest in chicks: behavioural and ecological aspects

    Behavior

    (2007)
  • O.R.J. Anderson et al.

    Global seabird bycatch in longline fisheries

    Endanger. Species Res.

    (2011)
  • M.J. Arnold et al.

    Albatross population in peril: a population trajectory for black-browed albatrosses at South Georgia

    Ecol. Appl.

    (2006)
  • J.A. Awkerman et al.

    Female-biased sex ratio arises after parental care in the sexually dimorphic waved albatross (Phoebastria irrorata)

    Auk

    (2007)
  • J.A. Awkerman et al.

    Isotopic (δ15N and δ13C) evidence for intersexual foraging differences and temporal variation in habitat use in waved albatrosses

    Can. J. Zool.

    (2007)
  • C. Barbraud et al.

    Effects of climate change and fisheries bycatch on Southern Ocean seabirds: a review

    Mar. Ecol. Prog. Ser.

    (2012)
  • J.A. Bartle

    Sexual segregation of foraging zones in procellariiform birds: implications of accidental capture on commercial fishery longlines of grey petrels (Procellaria cinerea)

    Notornis

    (1990)
  • J.A. Bartle

    Incidental capture of seabirds in the New Zealand subantarctic squid trawl fishery

    Bird Conserv. Int.

    (1991)
  • J. Beck et al.

    Necropsy Findings From Seabird Bycatch in Hawaii and Alaska Longline Fisheries: Examinations Conducted in 2013

    (2013)
  • P. Blanchard et al.

    Offspring sex ratio in relation to parental structural size and body condition in the long-lived wandering albatross (Diomedea exulans)

    Behav. Ecol. Sociobiol.

    (2007)
  • T. Bregnballe et al.

    Net-entrapment of great cormorants Phalacrocorax carbo sinensis in relation to individual age and population size

    Wildl. Biol.

    (2006)
  • V. Bretagnole et al.

    Method for sexing fledglings in Cory's shearwaters and comments on sex-ratio variation

    Auk

    (1995)
  • L. Bugoni et al.

    Age composition and sexual size dimorphism of albatrosses and petrels off Brazil

    Mar. Ornithol.

    (2009)
  • L. Bugoni et al.

    Sex-biased incidental mortality of albatrosses and petrels in longline fisheries: differential distributions at sea or differential access to baits mediated by sexual size dimorphism?

    J. Ornithol.

    (2011)
  • T. Burg

    Genetic analysis of wandering albatrosses killed in longline fisheries off the east coast of New Zealand

    Aquat. Conserv.

    (2008)
  • J.P. Croxall et al.

    Recoveries of wandering albatrosses Diomedea exulans ringed at South Georgia 1958–1986

    Ringing Migr.

    (1990)
  • J.P. Croxall et al.

    Population changes in albatrosses at South Georgia

  • J.P. Croxall et al.

    Seabird conservation status, threats and priority actions: a global assessment

    Bird Conserv. Int.

    (2012)
  • J. Croxall et al.

    Appropriate scales and data to manage seabird-fishery interactions: comment on Torres et al. 2013

    Mar. Ecol. Prog. Ser.

    (2013)
  • K. Delord et al.

    Seabird mortality in the Patagonian toothfish longline fishery around Crozet and Kerguelen Islands, 2001–2003

    CCAMLR Sci.

    (2005)
  • K. Delord et al.

    Multivariate effects on seabird bycatch in the legal Patagonian toothfish longline fishery around Crozet and Kerguelen Islands

    Polar Biol.

    (2010)
  • P.W. Dillinghan et al.

    Potential biological removal of albatrosses and petrels with minimal demographic information

    Biol. Conserv.

    (2011)
  • P.F. Donald

    Adult sex ratios in wild bird populations

    Ibis

    (2007)
  • A.K. Fridolfsson et al.

    A simple and universal method for molecular sexing of non-ratite birds

    J. Avian Biol.

    (1999)
  • P.A. Gandini et al.

    Spatial and temporal patterns in the bycatch of seabirds in the Argentinean longline fishery

    Fish. Bull.

    (2006)
  • P.A. Gandini et al.

    Interaction between Magellanic penguins and shrimp fisheries in Patagonia, Argentina

    Condor.

    (1999)
  • E. Gómez-Díaz et al.

    Geographic assignment of seabirds to their origin: combining morphologic, genetic, and biogeochemical analyses

    Ecol. Appl.

    (2007)
  • B.S. Halpern et al.

    A global map of human impact on marine ecosystem

    Science

    (2008)
  • A. Hedd et al.

    Seasonal sexual segregation by monomorphic sooty shearwaters Puffinus griseus reflects different reproductive roles during the pre-laying period

    PLoS One

    (2014)
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