Elsevier

Biological Conservation

Volume 252, December 2020, 108831
Biological Conservation

Perspective
Conservation challenges for the most threatened family of marine bony fishes (handfishes: Brachionichthyidae)

https://doi.org/10.1016/j.biocon.2020.108831Get rights and content

Highlights

  • Rare micro-endemic marine species face extreme conservation challenges.

  • Half of 14 known handfish species are now listed as threatened on the IUCN Red List.

  • The Smooth handfish is the first marine bony fish to be listed as Extinct.

  • Lack of a pelagic larval stage greatly increases extinction risk for handfishes.

  • Only four extant species of handfish have been observed in the last 20 years.

Abstract

Marine species live out-of-sight, consequently geographic range, population size and long-term trends are extremely difficult to characterise for accurate conservation status assessments. Detection challenges have precluded listing of marine bony fishes as Extinct on the International Union for Conservation of Nature (IUCN) Red List, until now (March 2020). Our data compilation on handfishes (Family Brachionichthyidae) revealed them as the most threatened marine bony fish family, with 7 of 14 species recently listed as Critically Endangered or Endangered. The family also includes the only exclusively marine bony fish to be recognised as Extinct – the Smooth handfish (Sympterichthys unipennis). Ironically, some of the characteristics that threaten handfishes with extinction have assisted assessments. Poor dispersal capabilities leading to small, fragmented populations allow monitoring and population size estimation for some shallow water species. Evidence that the Smooth handfish is now Extinct included no sightings over 200 years in an area subject to numerous scientific surveys, inferred shallow habitat and moderate abundance at time of original collection, and major habitat transformation through fishing, aquaculture, rising sea temperature, and urban development. Contemporary threats to extant handfish species include habitat degradation, introduced species, loss of spawning substrate, climate change, and demographic risks associated with small, fragmented populations. Multifaceted conservation efforts are needed, including addressing threats to habitat quality, bolstering wild population numbers, and implementing novel techniques to find and monitor populations. Expanded monitoring, including application of eDNA methods, represent critical steps towards overcoming the challenges in studying wild populations of rare marine species. Ongoing investigation will likely reveal numerous other threatened species for which little is known.

Introduction

Accurate reporting of the conservation status of marine fishes is generally extremely difficult, resulting in relatively few status assessments compared to other marine vertebrates and terrestrial animals (Reynolds et al., 2005). In addition to the usual monitoring challenges for rare species, search effort for marine species is limited by sea-state, vessel availability, and depth. For small, sea floor-dwelling marine animals, finding an individual can be akin to finding a needle in a haystack. This is no doubt a key reason for a lack of recognised extinctions in the marine realm (Edgar et al., 2017; McCauley et al., 2015; Reynolds et al., 2005), and high proportion of Data Deficient listings of marine species in the International Union for Conservation of Nature's (IUCN) Red List of Threatened Species.

Recent updates of the IUCN Red List have attempted to reduce this under-representation of marine threatened species, particularly fishes. The Red List now covers 20,341 of 35,423 described freshwater and marine fish species (Superclass Pisces; IUCN, 2020), of which 2721 (13% of assessed species) are considered threatened, and 74 are listed as Extinct or Extinct in the Wild. Until the 2020 update, none of the Extinct species was a marine bony fish.

The recent update covered all 14 species in the Family Brachionichthyidae (handfishes), a small group of marine fishes with distribution restricted to south-eastern Australia. Before this Red List update, only a single species from this family, the Spotted handfish (Brachionichthys hirsutus) had been assessed. Originally assessed in 1996, it was one of the first marine fishes to be listed as Critically Endangered, the highest level of extinction risk (Hudson and Mace, 1996). Excluding families that have not yet been completely assessed (and those in which only a single species has been assessed), the handfishes are now the most threatened marine bony fish family included on the IUCN Red List (Fig. 1), with 57% of its species listed as Critically Endangered, Endangered or Extinct. Brachionichthyidae is the 11th most threatened fish family containing largely marine members (only shark and ray families have a greater proportion of threatened members, Fig. 1). The primary goals of this study were to review the state of knowledge on the handfishes, including characteristics that have contributed to their extreme vulnerability, document the information basis for the Red List assessments, and discuss future directions for the conservation of handfishes and other small and inconspicuous marine species.

Handfishes are relatively small (60–151 mm) marine fishes with distributions restricted to the temperate waters of south-eastern Australia, predominantly concentrated in Tasmania (Last and Gledhill, 2009). The fossil record documents handfishes as well represented in the Eocene period (from 56 to 33 million years ago) in the Monte Bolca area of Italy, indicating that the family once occupied a vastly different, and likely larger, range of marine realms (Carnevale and Pietsch, 2010). Their very small present-day range in south-eastern Australia has been suggested as a residual distribution resulting from a range shift between West Tethyan and Indo Australian Archipelago hotspots (Carnevale and Pietsch, 2010).

Brachionichthyidae are the most speciose of the marine fish families entirely endemic to Australia, with almost half of the species exhibiting the narrowest geographic distributions of any of the 4000+ fish species found throughout the region (Bruce et al., 1998; Pogonoski et al., 2002; Fig. 3). The family comprises of 14 species (Last and Gledhill, 2009), most of which are poorly studied, particularly those restricted to greatest depths. The phylogenetic lineage has changed little morphologically since the early fossil records (Edgar et al., 2017; Last and Gledhill, 2009); they are demersal, generally cryptic in nature, with pectoral fin extremities reminiscent of human hands – hence their name (Carnevale and Pietsch, 2010; Whitley, 1949). Lacking a swim bladder, they prefer to use their ‘hands’ to ‘walk’ across the sea floor, rather than swim (although can do so over short distances when disturbed).

In the marine realm, the majority of listed threatened fishes belong to the class Chondrichthyes (sharks and rays), often because of life history characteristics that make them vulnerable, such as slow growth rates, delayed maturity, and smaller clutch/brood sizes (Musick, 1999). To date, no species of shark or ray is listed as Extinct, although several species have been extirpated from large parts of their range, and one species (the Clown wedgefish, Rhynchobatus cooki) is listed as Critically Endangered (Possibly Extinct) (Dulvy and Forrest, 2009; Simpfendorfer et al., 2011). Sawfishes (Pristidae), wedgefishes (Rhinidae) and giant guitarfishes (Glaucostegidae), which are targeted for their high-value fins, are among the most threatened families within the sharks and rays as well as across marine fish families of the world (Kyne et al., 2019).

Section snippets

Extinct – no reasonable doubt that the last individual has died

In 2020, the Smooth handfish (Sympterichthys unipennis), an Australian endemic marine species not seen in over 200 years, was the first marine bony fish worldwide to be formally classified as Extinct. This species is known from only the holotype individual (Fig. 2) obtained by French zoologist François Péron during an expedition to Australia in the early 1800s (Last and Gledhill, 2009). It is among the first endemic fish species described from Australia. This species was likely impacted by

Threats

Brachionichthyids have relatively few eggs (~50–150 for the three species for which this is known) and no planktonic larval stage, instead hatching as fully metamorphized juveniles that are inferred to directly recruit; consequently, dispersal is severely limited. Limited capture-mark-recapture work and genetics for the most extensively studied of the species, the Spotted handfish (B. hirsutus), also suggests very limited adult movements and genetic isolation between local populations, even

Conservation measures

Species extinctions result in the loss of biodiversity and natural heritage values, but may also have potential ecological consequences (Hooper et al., 2012; Ling et al., 2009). It is impossible to speculate on any potential ecological impacts associated with the loss of handfishes from the south-eastern Australian seascape, given the lack of ecological information about most species and their extreme contemporary rarity.

The IUCN Red List represents the most comprehensive information source on

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was supported by the Marine Biodiversity Hub, a collaborative partnership supported through funding from the Australian Government's National Environmental Science Programme (NESP). We thank divers from Reef Life Survey, the Institute for Marine and Antarctic Studies, and CSIRO who contribute to the monitoring Spotted and Red handfish populations, and the Derwent Estuary Program, Antonia Cooper, Ella Clausius, Mark Stalker, Karen Gowlett-Holmes, Mick Barron, Mark Green, Barry Bruce,

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