New opportunities for conservation of handfishes (Family Brachionichthyidae) and other inconspicuous and threatened marine species through citizen science

Abstract

Volunteer divers participating in the Reef Life Survey (RLS) program actively assist species conservation efforts by generating data for threat assessments and population trend monitoring, through in-water restoration efforts, and through outreach of marine conservation messages. Up to 2014, standardised underwater visual survey data provided by RLS divers described densities of 495 cryptic fish species at over 1200 sites distributed around Australia. Each species was recorded on 34 separate transect blocks on average, allowing the first assessments of population trends for many species. These data highlight the threatened and data deficient status of endemic Australian handfish species. At least five shallow-water handfish species are potentially threatened, including the smooth handfish Sympterichthys unipennis, which has not been sighted for over 200 years, but is yet to be included on any threatened species list. RLS divers undertook directed searches at key historical locations for two handfish species, the red handfish Thymichthys politus, now only known from a single reef, and Ziebell's handfish Brachiopsilus ziebelli, with no confirmed sighting for over a decade. From a total of 100 h of underwater search effort, only four red handfish were recorded, all at a site threatened by adjacent human activity. These and other handfish species should be considered for inclusion on the IUCN Red List given that populations are either very small or have vanished, spawning substrates have probably declined, and the species lack a larval dispersal stage. More importantly, the absence of information on the conservation status of the majority of marine species needs urgent attention, including through expanded citizen science efforts, if management intervention is to occur and extinctions minimised.

Introduction

Marine plants and animals are often considered to face much lower extinction risk than terrestrial taxa, a consequence inferred from high geographic connectivity associated with ocean currents, and generally wide geographic distributions. The low number of documented extinctions supports this contention. By contrast, objective assessment of extinction risk using the IUCN Red List of Threatened Species criteria (IUCN, 2001) indicates little difference in the proportion of threatened species identified for major marine and terrestrial taxa that have been comprehensively assessed at the global level. A total of 6%, 4%, and 13% of sharks and rays, corals, and marine mammals are considered threatened (Vulnerable, Endangered or Critically Endangered), compared to 6%, 12% and 13% for birds, reptiles and terrestrial mammals, while rates for species that move between land and sea are substantially higher (57%, 39% and 14% for sea turtles, amphibious mammals and seabirds, McCauley et al., 2015).

One difference between outcomes of terrestrial and marine Red List assessments is the proportion of species ranked as Data Deficient (DD). A total of 24% of assessed marine species are considered DD because of insufficient population information for a credible threat ranking, compared to 16% of assessed terrestrial species (IUCN Red List accessed 29 June 2015). Data on population trends in animals and plants are available for very few marine species (probably < 1% of the > 170,000 described species, Mora et al., 2011), confounding threat assessments.

General ignorance about the threat status of marine species is highlighted by an iconic group of Australian marine fishes, the handfishes belonging to the family Brachionichthyidae. This is by far the largest fish family wholly confined to Australian waters, with 14 species recognised, most with localised distributions in Tasmania and southeastern Australia. Handfishes are colourful, crawl in preference to swim, lack a pelagic stage in the life-cycle, and possess an ancient phylogenetic lineage, with little morphological change since the fossil species Histionotophorus bassanii was deposited in early Eocene rock strata in Italy ~ 50 million years ago (Last and Gledhill, 2009).

While many handfish specimens were observed in the 19th and 20th centuries, few handfishes have been observed in recent decades (Table 1). The best known species is the spotted handfish (Brachionichthys hirsutus), the first marine fish to be classed by the Australian Government as Critically Endangered (CR), following a rapid population decline around 1980. While the ultimate cause of the population decline remains unknown, potential factors include predation of eggs by the introduced Northern Pacific seastar (Asterias amurensis), lack of available habitat structure for deposition of eggs, and poor environmental condition throughout the current known range of the species at the mouth of the Derwent Estuary near Hobart (Edgar, 2008). The total population size of this species has been estimated to be several thousand individuals (Department of the Environment and Heritage, 2004).

While scientific interest has focused primarily on the spotted handfish, other handfish species are probably closer to extinction (Table 1), including the red handfish (Thymichthys politus) and Ziebell's handfish (Brachiopsilus ziebelli), which are listed as Critically Endangered and Vulnerable, respectively, under the Australian Environmental Protection and Biodiversity Conservation Act (Commonwealth of Australia, 2015). Neither is included on the IUCN Red List, yet both have declined greatly in range over the past century, with only one small population of a few individuals known for the red handfish, and no Ziebell's handfish reported for over a decade. Another endemic Tasmanian handfish species, the pink handfish (Brachiopsilus dianthus) has not been seen for over 20 years, and is not on any threatened species list. This is also the case for the smooth handfish (Sympterichthys unipennis), a species once sufficiently abundant to be collected in Tasmania by early French naturalists with simple sampling gear, but which has not been seen for over 200 years. If this was a mammal, bird, reptile, frog or plant species, then it would be listed on the IUCN Red List and Australian threatened species lists as Extinct, but as a poorly known marine species, it has not yet been considered for any listing.

The pivotal issue associated with assessing the true population status of most marine species, and evaluating the state of the marine environment more generally, is that the marine realm lies out of sight and is expensive to survey. Nevertheless, the limited available information unambiguously suggests that major environmental problems exist and need urgent attention. Threats associated with climate change, introduced pests, fishing, and pollution are serious and pervasive, and populations of many taxa are declining rapidly worldwide, including large fishes, higher vertebrates and sea stars (Jackson et al., 2001, Stokstad, 2014). Marine ecosystems declining globally as a consequence of human activity include coral reefs (Carpenter et al., 2008), seagrass beds (Waycott et al., 2009), mangroves (Sandilyan and Kathiresan, 2012), shellfish reefs (Beck et al., 2011), kelp forests (Dayton et al., 1998), and pelagic systems (Boyce et al., 2010). Moreover, analysis of historically-dated mollusc shell fragments indicates marine biodiversity can collapse catastrophically at the regional scale with no public or scientific observation (Edgar and Samson, 2004).

Using the Reef Life Survey (RLS) program as a case example, this study outlines the potential for citizen science to transform threat assessment and conservation management of shallow-water marine species. The RLS model of utilising a skilled team of committed divers who donate their time and expertise, but without sacrificing scientific rigour, allows enhanced survey effort for rare and threatened species such as handfishes. By contrast, professional scientists are unlikely to receive sufficient funding to track population trends of thousands of marine species across continental scales through the long term, as is needed for informed management.

The RLS program was established through a pilot project hosted within the Commonwealth Environmental Research Facilities program from 2007 to 2010, which successfully achieved collection of quantitative data over the continental scale, without sacrificing taxonomic resolution and other detail. Subsequently, the non-profit Reef Life Survey Foundation (http://www.reeflifesurvey.com/) was formed to train committed divers in systematic underwater visual census surveys, refine data entry procedures, and operate ongoing field activities through a combination of targeted field campaigns and ad-hoc surveys of local and vacation sites by trained divers. More than 100 active RLS divers participate at present, and standardised, quantitative data have been collected at > 3000 sites in 43 countries worldwide, including > 500,000 abundance records for > 4500 species. Many sites have been surveyed on multiple occasions, in some cases annually each year since 2008. Survey numbers continue to grow.

Reef Life Survey methods are based on visual census techniques applied over two decades by University of Tasmania and tropical eastern Pacific researchers (Barrett et al., 2007, Edgar et al., 2011). They cover multiple important elements of biodiversity quantified along transect lines set on subtidal rocky and coral reefs: fishes, large mobile macroinvertebrates, sessile invertebrates, and macroalgae. Surveys include searching for small, camouflaged, or otherwise inconspicuous fish species closely associated with the bottom, which may otherwise be overlooked (hereafter referred to as cryptic fishes, see Supplementary Table 1). These are counted along 1-m wide 50-m long belts during close searches of the reef surface.

This study provides an overview of how conservation of handfishes and other cryptic fishes is assisted by RLS volunteers through:

• Standardised surveys of the subset of cryptic fishes that is detectable by divers during seabed searches, including handfishes;

• Targeted searches for threatened handfishes at historical locations where populations are most likely to persist; and

• On-ground action in support of management intervention.

This assistance aligns with management priorities and is supported by national and state conservation authorities. In particular, the Australian Government Recovery Plan for Three Handfish Species identifies, amongst others, the following priority actions, where assistance by citizen scientists is fundamental (Commonwealth of Australia, 2015):

• Monitor the populations and determine population size and rates of population change, by undertaking scientifically robust and repeatable population surveys;

• Identify important habitat areas and assess their quality;

• Where suitable spawning substrate for these species is lacking, encourage the introduction and maintenance of artificial spawning substrate and/or natural spawning substrate to increase reproductive success;

• Promote community awareness of the value of handfishes as part of Australia's unique biodiversity.