Reproductive biology of the two deep-sea chimaerids, longnose spookfish (Harriotta raleighana) and Pacific spookfish (Rhinochimaera pacifica)

Highlights

• Reproductive biology of two poorly known deep-sea chimaeras H. raleighana and R. pacifica is described.

• Both species matured at a large proportion of their maximum length, suggesting late maturation.

• Sperm storage tubules (SSTs) and sperm bundles were identified in the terminal zone of the oviducal gland.

• Sexual dimorphism in snout length was found in H. raleighana, suggesting the snout is a male secondary sexual characteristic.

• All known publications on holocephalan reproduction are reviewed.

Abstract

The family Rhinochimaeridae, the long-nose chimaerids, consists of eight species across three genera, two of which occur in New Zealand waters. Very little is known about the biology of the rhinochimaerids. Longnose spookfish, (Harriotta raleighana, Goode and Bean, 1895), and Pacific spookfish, (Rhinochimaera pacifica, Mitsukuri, 1895), were collected from research trawl surveys and by commercial fishing vessels around New Zealand at depths between 400 and 1300 m. A total of 300 H. raleighana were caught which varied in length from 18.7 to 90.4 cm chimaera length (CL), and 168 R. pacifica at lengths of 20.9–139.9 cm CL. External assessment of male claspers and female gonad mass and oviducal gland width were the best indicators for maturity. Both species matured at a large proportion of their maximum length. Length at maturity was estimated at 62.8 cm CL and 75.8 cm CL for male and female H. raleighana respectively, and 105.3 cm CL and 125.0 cm CL for male and female R. pacifica. Fecundity was low and measured up to 27 eggs for H. raleighana, and 31 eggs for R. pacifica. Sperm storage was confirmed in females of both species. Sexual dimorphism in snout length was found in H. raleighana, where male relative snout size increased at sexual maturity, suggesting the snout is a secondary sexual characteristic. This study contributes to a better understanding of the life histories of H. raleighana and R. pacifica and their vulnerability to exploitation as fisheries bycatch.

Introduction

Chimaerids, also known as ratfish or ghostsharks, form the subclass Holocephali, and along with Elasmobranchii (sharks and rays), make up the class Chondrichthyes (Didier, 1995). The holocephalan family Rhinochimaeridae is globally distributed, consisting of eight species across three genera, and are distinguished from other chimaerids by having long tapered snouts. The longnose spookfish (Harriotta raleighana, Goode & Bean, 1895) is the only chimaerid with a presumed worldwide distribution (Didier et al., 2012). It is relatively common across the continental shelf and ocean floor of the Northern Atlantic, as well as the Northwest and Southwest Pacific (Last and Stevens, 2009). The Pacific spookfish (Rhinochimaera pacifica, Mitsukuri 1895) has a patchy known distribution on the continental shelf of the Pacific and Indian Oceans (Didier and Nakaya, 1999), with reports across the Japanese Archipelago to the South China Sea (Shao and Hwang, 1997, Shinohara et al., 2009), Australia (Last and Stevens, 2009), New Zealand (McMillan et al., 2011), and Peru (Chirichigno, 1974). Around New Zealand, both species are widely distributed on the continental shelf at depths from 400 to 1300 m (Inada and Garrick, 1979; McMillan et al., 2011), with R. pacifica typically found deeper than H. raleighana (Dunn et al., 2010). Elsewhere, H. raleighana has been recorded at depths up to 2600 m (Priede et al., 2006).

Harriotta raleighana and R. pacifica are listed as Least Concern by the International Union for the Conservation of Nature (IUCN), but very little is known about their biology. This is largely due to a lack of targeted sampling and taxonomic confusion (Kyne and Simpfendorfer, 2007, Holt et al., 2013). Chimaerids that have been studied have expressed K-selected characteristics similar to deep-sea elasmobranchs (relatively slow growth, high longevity, late maturation, low fecundity see Barnett et al., 2012; King and McPhie, 2013). These factors, along with their tendency to aggregate (Barnett et al., 2012, Quinn et al., 1980) and distribution overlap with fishing effort (Bagley et al., 2013), make chimaerids susceptible to overfishing.

Harriotta raleighana has been reported to grow to a length of 120 cm, although it has never been recorded larger than 90 cm in New Zealand, and R. pacific to 165 cm (McMillan et al., 2011). Both species are oviparous, and it is likely that individual embryos contained in an egg case are deposited onto the ocean floor as exhibited by other chimaerids (Dean, 1906, Didier et al., 2012). Gestation for chimaerids may last up to 8 months (Barnett et al., 2009), and one report estimated size at birth for H. raleighana to be between 10 and 13 cm (Cox and Francis, 1997). Based on preserved specimens, size at maturity for H. raleighana has previously been estimated between 25 and 30 cm body length (BDL, dorsal edge of gill opening to origin of upper caudal fin) for males and 35 cm BDL for females, and at 50 cm BDL for R. pacifica (Didier, Millersville University, pers. comm).

Biomass estimates show no trends for H. raleighana and R. pacifica (O’Driscoll et al., 2011, Bagley et al., 2013). Nevertheless, there are many documented instances of declining trends in abundance of deep-sea taxa as a result of fishing (Heymans et al., 2010, Norse et al., 2012), and chimaerid populations could be negatively affected with expanding deep-sea fisheries (Simpfendorfer and Kyne, 2009). No target fisheries for H. raleighana or R. pacifica exist in New Zealand, but both are caught as bycatch in deep-sea trawl fisheries (Jacob et al., 1998, Allain et al., 2003, Ministry for Primary Industries, 2015). Harriotta raleighana is caught regularly in New Zealand waters, making it one of the most common bycatch species that is not managed by the fisheries Quota Management System (QMS). An estimated catch of 82 t was recorded between the 2008–09 and 2012–13 fishing years (Ford et al., 2015). In contrast, R. pacifica is only occasionally caught as bycatch, with less than 5 t of estimated catch between the 2008–09 and 2012–13 fishing years (Ford et al., 2015). It is also occasionally recorded by the Ocean Trawl Fishery of Australia at midslope depths of 760–1290 m (Pethybridge et al., 2012).

The purpose of this research was to quantify reproductive parameters to investigate the reproductive biology of H. raleighana and R. pacifica, and determine if these species possess the same biological characteristics that make other deep-sea chondrichthyan vulnerable to overfishing. To add in this comparison, we also review other studies that focused on holocephalan reproductive biology, expanding previous work by Kyne and Simpfendorfer (2007).