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Hippocampus whitei Bleeker, 1855, a senior synonym of the southern Queensland seahorse H. procerus Kuiter, 2001: molecular and morphological evidence (Teleostei, Syngnathidae)
expand article infoGraham Short, David Harasti§, Healy Hamilton|
‡ California Academy of Sciences, San Francisco, United States of America
§ Fisheries Research, Port Stephens Fisheries Institute, Port Stephens, Australia
| NatureServe, Arlington, United States of America
Open Access

Abstract

The taxonomic status of the seahorse Hippocampus procerus Kuiter, 2001, type locality Hervey Bay, QLD, Australia, was re-examined based on its strong morphological similarity and geographical proximity to its congener H. whitei Bleeker, 1855, a species recorded in ten estuaries of New South Wales, Australia. Kuiter (2001) distinguished H. procerus from H. whitei by a taller coronet, marginally lower meristics, and spinier physiognomy. Meristic, morphometric, and key diagnostic morphological character comparisons from vouchered specimens of the two purported species collected from Sydney Harbour, Nelson Bay, Port Stephens, NSW and Hervey Bay, Bundaberg, and Moreton Bay, QLD did not show diagnostic differences to support species-level classification of H. procerus. Furthermore, partial mitochondrial COI sequence data from specimens sampled from known geographical distributions in NSW and Southport, QLD failed to discriminate between populations as a result of shared haplotypes, and revealed an average intraspecific divergence of 0.002%. Hippocampus procerus is hereby placed in the synonymy of H. whitei; a redescription is provided, with a revised record of its range across eastern Australia.

Keywords

Acanthomorpha, Australia, COI, marine fish, morphology, systematics, taxonomy

Sea-horse, or Hippocampus. This animal, like the Flying-fish, being commonly known, a description is not necessary. It is the Syngnathus Hippocampus of Linnaeus. See plate 264” (White 1790: 295).

Introduction

Hippocampus whitei Bleeker, 1855, is a geographically restricted species of seahorse recorded in ten coastal estuaries and embayments of central New South Wales (NSW), and also farther north in the Tweed River, Australia. It can be found occurring in a variety of habitats including seagrasses, soft corals, sponge gardens, and artificial structures to depths of 15 m (Vincent et al. 2004; Hellyer et al. 2011; Harasti et al. 2014a). It is listed as ‘Endangered’ under criterion A2bc of the IUCN Red List due its restricted distribution, loss of essential marine habitats, and associated population declines in developed urban estuaries, including Port Stephens and Sydney Harbour (Harasti 2016; Harasti and Pollom 2017). Therefore, the conservation of H. whitei populations through the implementation of species monitoring and various management options, such as habitat protection and no-take policies are important for their protection and recovery, as well as for scientific, ecological, and economic purposes (Harasti et al. 2010, 2012, 2014b; Hellyer et al. 2011; Vincent et al. 2011).

Efforts to advance the conservation of seahorse populations are highly dependent on being able to confidently identify individual species in and beyond their known geographic distributions. The most recent and comprehensive taxonomic review of the genus Hippocampus (Lourie et al. 2016) places the number of recognized seahorse taxa occurring in Australia at sixteen species. However, the validity of several putative species remains uncertain. Seahorses are challenging to identify: multiple species have been synonymized based on recent genetic data, and there are many previous descriptions now recognized as spurious misidentifications attributed to the use of unreliable or non-diagnostic morphological characters (Lourie et al. 2016).

The taxonomic identity of Hippocampus procerus Kuiter, 2001, originally described from Hervey Bay, Queensland (QLD), with a known distribution in Gold Coast Seaway and Moreton Bay, QLD, has been in question due to its strong morphological similarity and geographic proximity to H. whitei (Lourie et al. 2016). It was distinguished from H. whitei primarily by a taller coronet, subtle differences in meristic characters, and a spinier physiognomy (Kuiter 2001). These indistinct morphological differences between the two species prompted a re-examination of the holotype and non-type specimens of H. procerus from Hervey Bay, paratypes of H. procerus from Bundaberg and Moreton Bay, QLD, non-type specimens of H. procerus from Mackay, Elliot Heads, and Gold Coast Seaway, QLD, and non-type specimens of H. whitei from Sydney Harbour and Nelson Bay, Port Stephens, NSW, employing meristic, morphometric, and key diagnostic morphological character comparisons. The diagnostic characters comprise in part the absence or presence of principal spines, including snout, cleithral ring, neck, and subdorsal spines, with respect to their spatial position on the head and body. We demonstrated that the morphological characters in the non-type specimens of H. whitei corresponded closely with the examined non-type specimens, paratypes, and the holotype specimen of H. procerus, including: coronet height, absence of neck spines, indiscernible or small parietal spine, the numbers and positions of cleithral ring and subdorsal ridge spines, and overall spine physiognomy. Partial mitochondrial COI sequence data generated from specimens sampled from known geographical distributions in NSW and from Southport, QLD failed to discriminate between populations as a result of shared haplotypes, and revealed an average intraspecific divergence of 0.002%. Hippocampus whitei Bleeker, 1855, is herein formally redescribed as a senior synonym of H. procerus. This estuarine species is apparently endemic to estuaries of central NSW, the Tweed River, and southern QLD.

Materials and methods

Four individuals referred to as H. procerus, based on known locality of this species (Kuiter 2001), were collected from Southport, Gold Coast Harbour, QLD in 2014 by seine in seagrass beds in 1–2 m depth or by hand nets while scuba diving in less than 8 m depth (Figure 1), from which tissue was sampled from the caudal tip of the tails and preserved in a NaCl-saturated DMSO solution for genetic analyses. Similarly, thirty-one individuals of H. whitei were tissue sampled from the caudal tip of the tail at seven localities along the species’ known geographic range in New South Wales, Australia (Table 1, Figure 1) from 2007–2009. DNA extraction, PCR amplification, alignment, and analysis of partial mitochondrial cytochrome c oxidase subunit I (COI) sequences was performed following standard protocols described in Hamilton et al. (2017). Genetic distances (uncorrected p-distances) were calculated and neighbour-joining (NJ) trees constructed with confidence levels assessed using 1000 bootstrap replications based on partial COI using MEGA v. 7.0.26 (Kumar et al. 2017).

List of H. whitei specimens, and those referred to as H. procerus, including collection locality, voucher or field number, and COI GenBank accession numbers.

Species Locality Voucher / Field COI GenBank accession no.
1 Hippocampus procerus Southport, QLD, Australia CAS 241511 MH745371
2 Hippocampus procerus Southport, QLD, Australia CAS 241512 MH745372
3 Hippocampus procerus Southport, QLD, Australia CAS 241513 MH745373
4 Hippocampus procerus Southport, QLD, Australia CAS 241514 MH745374
5 Hippocampus whitei Sydney, NSW, Australia HH-0418 MH745375
6 Hippocampus whitei Sydney, NSW, Australia HH-0419 MH745376
7 Hippocampus whitei Sydney, NSW, Australia HH-0469 MH745377
8 Hippocampus whitei Sydney, NSW, Australia HH-0470 MH745378
9 Hippocampus whitei Sydney, NSW, Australia HH-0667 MH745379
10 Hippocampus whitei Empire Bay, NSW, Australia HH-1276 MH745380
11 Hippocampus whitei Empire Bay, NSW, Australia HH-1277 MH745381
12 Hippocampus whitei Nelson Bay, NSW, Australia HH-1287 MH745382
13 Hippocampus whitei Tuggerah Lake, NSW, Australia HH-1290 MH745383
14 Hippocampus whitei Tuggerah Lake, NSW, Australia HH-1291 MH745384
15 Hippocampus whitei Tuggerah Lake, NSW, Australia HH-1292 MH745385
16 Hippocampus whitei Nelson Bay, NSW, Australia HH-1295 MH745386
17 Hippocampus whitei Nelson Bay, NSW, Australia HH-1299 MH745387
18 Hippocampus whitei Nelson Bay, NSW, Australia HH-1300 MH745388
19 Hippocampus whitei Nelson Bay, NSW, Australia HH-1305 MH745389
20 Hippocampus whitei Port Hacking, NSW, Australia HH-1321 MH745390
21 Hippocampus whitei Port Hacking, NSW, Australia HH-1322 MH745391
22 Hippocampus whitei Port Hacking, NSW, Australia HH-1329 MH745392
23 Hippocampus whitei Port Hacking, NSW, Australia HH-1330 MH745393
24 Hippocampus whitei Port Hacking, NSW, Australia HH-1340 MH745394
25 Hippocampus whitei Port Hacking, NSW, Australia HH-1341 MH745395
26 Hippocampus whitei Nelson Bay, NSW, Australia HH-1352 MH745396
27 Hippocampus whitei Nelson Bay, NSW, Australia HH-1353 MH745397
28 Hippocampus whitei Nelson Bay, NSW, Australia HH-1354 MH745398
28 Hippocampus whitei Nelson Bay, NSW, Australia HH-1357 MH745399
30 Hippocampus whitei Nelson Bay, NSW, Australia HH-1359 MH745400
31 Hippocampus whitei Forster, NSW, Australia HH-1363 MH745401
32 Hippocampus whitei Nelson Bay, NSW, Australia HH-1364 MH745402
33 Hippocampus whitei Nelson Bay, NSW, Australia HH-1365 MH745403
34 Hippocampus whitei Forster, NSW, Australia HH-1366 MH745404
35 Hippocampus whitei Forster, NSW, Australia HH-1367 MH745405
36 Hippocampus whitei Forster, NSW, Australia HH-1368 MH745406
Figure 1. 

Collection locations for H. procerus in QLD and H. whitei in NSW, Australia.

Proportional measurements and counts based on eight morphometric and six meristic variables (Tables 2, 3), including 17 diagnostic morphological characters, were performed on dried or ethanol-preserved specimens and high-resolution digital images of specimens using ImageJ (Rasband et al. 1997) to the nearest 0.1 mm following Lourie and Randall (2003) and Lourie and Kuiter (2008). External morphological characters were documented using a dissecting microscope or on high-resolution digital images of specimens. The holotype specimen of H. whitei is unknown. The original description of H. whitei Bleeker, 1855 is based on an artistic and non-informative rendering (White 1790: 264, plate 50) from Sydney Harbour, NSW. Morphometric measurements were recorded for two non-type specimens of H. whitei from Nelson Bay, NSW, two non-type specimens of H. procerus from Southport, Gold Coast Harbour, QLD, two non-type specimens of H. procerus from Moreton Bay, QLD, and one non-type specimen of H. procerus from Bundaberg and Mackay, QLD, respectively (Table 2). These data were compared to morphometric data from the holotype specimen of H. procerus from Hervey Bay, QLD (Table 2). Meristic counts and diagnostic morphological characters were recorded for 12 non-type specimens of H. whitei, including two from Sydney Harbour, six from Pittwater, and four from Nelson Bay, NSW, and 13 type and non-type specimens of H. procerus, including four from Southport, Gold Coast Harbour, QLD, two from Moreton Bay, one from Hervey Bay, QLD, one from Elliot Bay, four from Bundaberg, and one from Mackay, QLD (Table 3). These data were compared with similar morphological data (Table 3) for the holotype specimen of H. procerus from Hervey Bay, QLD.

Counts and morphometric measurements of specimens of H. whitei from Nelson Bay, NSW and those referred to as H. procerus from Southport, Moreton Bay, and Hervey Bay, QLD. Abbreviations: SnD (snout depth), SnL (snout length), CH (coronet height), HL (head length), HD (head depth), PO (post-orbital length), TrL (trunk length), TaL (tail length), SL (standard length). Numbers separated by a colon represent proportions (%). Lines present, from top to bottom, counts for trunk rings, tail rings, subdorsal rings, dorsal and pectoral fin rays.

H. whitei H. whitei H. procerus H. procerus H. procerus H. procerus H. procerus H. procerus H. procerus
Voucher or field number PSFC-DH-1 PSFC-DH-2 CAS 241511 CAS 241512 QM I.30772 AMS I.12554 AMS E2914 CAS-SU 36420-3 CAS-ICH 13406
Type status non-type non-type non-type non-type Paratype Paratype Holotype non-type non-type
Sex adult male subadult female adult female juvenile female subadult female adult male adult female subadult female adult male
Location Nelson Bay, NSW Nelson Bay, NSW Southport, QLD Southport, QLD Morerton Bay, QLD Morerton Bay, QLD Hervey Bay, QLD Bundaberg, QLD Mackay, QLD
Trunk rings 11 11 11 11 11 11 11 11 11
Tail rings 34 34 35 35 34 35 35 35 35
Subdorsal rings 3 3 3 3 3 3 3 3 3
Dorsal fin rays 17 17 18 18 18 18 18 18 18
Pectoral fin rays 16 16 16 16 16 16 18 17 18
SL (mm) 142.7 47.7 122.1 58.5 95.0 105.0 123.3 124.7 113.4
SnD:SnL 23.9 24.9 24.2 27.6 28.7 23.9 31.2 21.9 23.5
CH:HL 45.5 46.5 45.1 47.8 52.9 48.9 44.8 50.8 46.7
HD:HL 57.0 60.6 55.6 60.4 48.4 52.4 47.8 47.0 49.5
SnL:HL 46.2 45.5 43.6 46.2 49.3 44.3 43.6 48.9 46.1
PO:HL 33.8 37.0 40.6 38.1 38.9 36.7 36.8 34.9 33.8
HL:SL 22.9 20.3 21.5 24.2 27.3 25.7 25.2 22.6 21.9
TrL:SL 41.4 29.3 33.8 39.1 45.7 37.6 39.3 31.8 38.7
TaL:SL 58.6 50.5 66.2 60.9 63.8 62.5 60.7 65.26 54.8

Comparison of diagnostic morphological characters in non-types specimens of H. whitei from NSW and non-type and type specimens of H. procerus from QLD.

H. whitei H. whitei H. whitei H. procerus H. procerus H. procerus H. procerus H. procerus H. procerus H. procerus
Voucher number CAS-SU 36407 CAS-SU 36417 PSFC-DH CAS 24151- 14 QM I.30772 AMS I.12554 AMS E2914 QM I.39230 CAS-SU 36420-2,3,4 CAS-ICH 13406-1
Type status non-type non-type non-type non-type Paratype Paratype Holotype non-type Paratype non-type
Location Port Jackson, NSW Port Hacking, NSW Nelson Bay, NSW Southport, QLD Moreton Bay, QLD Moreton Bay, QLD Hervey Bay, QLD Elliot Heads, QLD Bundaberg, QLD Mackay, QLD
Number of specimens 2 6 4 4 1 1 1 1 4 1
Coronet distinct and tall
Neck spines absent absent/present absent
Upper cleithral spine present
Mid cleithral spine present
Ventral cleithral spine present (single or double) present (single)
Upper cleithral spine position near top of pectoral fin base
Mid cleithral spine position near bottom of pectoral fin base
Ventral cleithral spine position ventral extent of head
Subdorsal rings spines 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0 3/0,1,0
Parietal spine absent or blunt absent or blunt absent or blunt absent or blunt absent or blunt absent or blunt absent or blunt absent or blunt absent/blunt/present present
Lateral head spine present
Snout spine present
Dorsal eye spine present (single) present (one paratype double) present (single)
Small posterior eye spine present
Superior trunk ridge spines enlarged 1,8 1,8 1,8 1,8 1,8 1,7,8,9 1,7,8,9 1,8 1,8 - 1,7,8,9 1,4,6,7,8,9
Lateral trunk ridge spines enlarged 8–11 8–11 8–11 8–11 8–11 8–11 2–11 6–11 2–11 4–11
Inferior trunk ridge spines enlarged 4–11 4–11 4–11 4–11 4–11 4–11 4–11 5–11 5–11 5–11
Superior tail ridge spines enlarged 1–12 1–12 1–12 1–12 1–12 1–12 1–13 1–10 1–10 1–12
Inferior tail ridge spines enlarged 1–8 1–8 1–8 1–8 1–8 1–9 1–7 1–10 1–10 1–5

Taxonomy

Hippocampus whitei Bleeker, 1855

Figures 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, Tables 1, 2, 3, 4, 5, 6 Common names: White’s seahorse; New Holland seahorse; Sydney seahorse (Australia)

Hippocampus novaehollandiae Steindachner, 1866: 474 (Sydney Harbour, Australia).

Hippocampus procerus Kuiter, 2001: 328–329, figs. 4, 40 (Hervey Bay, Queensland, Australia).

Material examined

CAS 241511, adult female, Wave Island, Southport, QLD, Australia, 27°55'56.2"S 153°25'08.4"E, 5 m depth, in seagrass bed, November 27, 2014; CAS 241512, juvenile female, South West Wall, Southport, QLD, Australia, 27°56'32.7"S 153°25'14.7"E, 5 m depth, rocks and sand, November 26, 2014; CAS 241513, adult male, South West Wall, Southport, QLD, Australia, 27°56'32.7"S 153°25'14.7"E, 5 m depth, rocks and sand, November 26, 2014; CAS 241514, subadult male, Broadwater, QLD, Australia, 27°57'09.3"S 153°24'37.0"E, in seagrass bed, November 27, 2014; PSFC-DH (Port Stephens Fisheries Centre NSW field designation), 4 specimens in lot, PSFC-DH-1 adult male, PSFC-DH-2, subadult female, Nelson Bay, NSW, Australia, 32°42'59.9"S 152°08'57.2"E, 7 m depth, sandy rubble and seagrass, 2007-2016; SU 36407, 2 specimens in lot, adult males, Port Jackson, NSW, Australia, 33°50'42.6"S 151°14'50.5"E; SU 36417, 6 specimens in lot, Port Hacking, Gunnamatta Bay, NSW, Australia, 34°03'50.0"S 151°08'39.0"E, October 30,1939; QM I.30772, subadult female, Chain Banks, Moreton Bay, QLD Australia, J Johnson, dredge, depth 3–7 m, January 24, 1997; AMS I.12554, adult male, Moreton Bay, QLD Australia, Amateur Fishermans Association of Qld, 1912; CAS 13406, 2 in lot, 13406-1 adult male, 13406-2 juvenile female, Mackay, QLD, Australia, 21°09'48.1"S 149°12'58.2"E, 11 m depth, July 12, 1939; SU 36420, 4 in lot, 36420-1 adult female, 36420-2, adult male, 36420-3 adult female, 36420-4 adult female, 4 miles east of Burnett R, Queensland, Australia, 25°20'21.0"S 151°52'41.7"E, 18 m depth, September 14, 1938; QM I.39230, subadult male, 2 miles NE of Elliot Heads, QLD, 24°55'00.0"S 152°31'00.0"E, March 4, 1982, trawl; QM I. 39656, adult female, east of Waddy Point, 24°58'36.0"S 153°24'08.4"E, March 26, 2005, trawl; CAS-SU 35442, 2 specimens in lot, F43-A adult female, F43-C adult male, Corny Point, South Australia, 34°54'38.7"S 137°03'35.7"E, October 31, 1912; AMS E2914, female holotype, 120 mm, 5–11 km east of Hervey Bay, Fairway Buoy, QLD, Australia, 25°8'59.64"S 152°50'26.94"E, FIS Endeavour, July 7, 1910; AMS IA4205, juvenile female, height 57 mm, Port Curtis, QLD, Australia, 23°55’S 151°23’E, dredged, M Ward & W Boardman, December 14, 1929.

Diagnosis

Hippocampus whitei differs from its congeners by the following combination of characters: trunk rings 11; tail rings 34–35; dorsal fin rays 17–18; pectoral fin rays 16; subdorsal rings three; subdorsal spines four, superior trunk ridge ending with three enlarged spines, superior tail ridge commencing with one enlarged spine (3/0,1,0); cleithral ring spines three, one small spine at each end of pectoral-fin base but none at gill-opening, large single or double spine at ventral extent of head; small lateral head spines, two, one directly posterior of eye, one anterodorsally of operculum and ventral of coronet; distinct snout spine; parietal spine, diminutive or absent; single eye spine, large, protruding dorsally; small single or double spine, rugose, posteroventrally of eye; coronet, distinct and tall, protruding anteriorly in juveniles, angled dorsoposteriorly in adults, five small spines present on apex in a star-like arrangement; superior trunk with enlarged spines on 1st and 8th tail ridges.

Redescription

General body shape as in Figs 211. Morphometric and meristic characters are listed in Table 2. Coronet distinct and tall, coronet height 44.8–47.89% in HL, protruding anteriad in juveniles, angled dorsoposteriorly in adults; bilateral gill-openings ventral of coronet; dorsal fin rays 17–18; pectoral fin rays 16; subdorsal rings three; dorsal fin base starting immediately posterior to ninth trunk ring and ending immediately posterior to first tail ring; trunk rings 11; tail rings 34–35. Body spines: coronet with five small spines present on apex in a star-like arrangement; neck spines absent; prominent spine dorsally of eye, small single or double spine, rugose, ventroposteriorly of eye; small lateral head spines, two, one directly posterior of eye, one anterodorsally of operculum and ventral of coronet; cleithral ring spines three, one small spine at each end of pectoral-fin base but none at gill-opening, large single or double spine at ventral extent of head; distinct snout spine on midline between eyes; parietal spine, diminutive or absent in adults, present in juveniles and subadults; subdorsal spines four, superior trunk ridge ending with three enlarged spines, superior tail ridge commencing with one enlarged spine (3/0,1,0); superior trunk with enlarged spines on 1st and 8th tail ridges observed in adults, on 1st , 7th, 8th, and 9th tail ridges observed in subadults; lateral trunk ridge with small spines on 2nd–11th trunk rings; inferior trunk ridge with small spines beginning on 5th trunk ring and ending on 11th trunk ring; superior tail ridge spines well developed anteriorly, becoming smaller posteriorly, with enlarged spines on 1st–12th tail rings; inferior tail ridge spines well developed anteriorly, becoming smaller posteriorly, with enlarged spines on 1st–8th tail rings; caudal fin absent in juveniles and adults.

Figure 2. 

Comparison of non-type specimens of AHippocampus procerus CAS 241511, preserved adult female, 142.7 mm SL, Southport, QLD B Hippocampus procerus CAS 241512, preserved juvenile, 112.7 mm SL, Southport, QLD 1 Hippocampus whitei PSFC-DH-1, preserved adult male, 122.1 mm SL, Nelson Bay, NSW D Hippocampus whitei CAS PSFC-DH-2, preserved subadult female, 47.7 mm SL, Nelson Bay NSW. Note the differences in coronet profile between juvenile/subadult and adult: projecting anteriad in juvenile/subadult versus lower or projecting posteriorly in adults.

Figure 3. 

Hippocampus whitei in situ, adult female, Nelson Bay, NSW, Australia at 5 m depth (photograph David Harasti).

Figure 4. 

Hippocampus whitei in situ, adult female, Gold Coast, QLD, Australia at 5 m depth (photograph David Harasti).

Figure 5. 

Hippocampus procerus, AMS E2914, adult female, holotype, 120 mm SL, Hervey Bay, Queensland, Australia (photograph Mark Allen).

Figure 6. 

Hippocampus procerus, QM I.30772, subadult female, paratype, 95.0 mm SL, Moreton Bay, Queensland, Australia (photograph Jeff Johnson).

Figure 7. 

Hippocampus procerus, AMS I.12554, adult male, paratype, 105 mm SL, Moreton Bay, Queensland, Australia (photograph Kerryn Parkinson).

Figure 8. 

Hippocampus procerus, QM I.39230, adult male, non-type, Elliot Heads, Queensland, Australia (photograph Jeff Johnson).

Figure 9. 

Hippocampus procerus, CAS-SU 36420, 4 specimens in lot, paratypes, Burnett River, Queensland, Australia (photograph Jon Fong).

Figure 10. 

Hippocampus procerus, CAS-ICH 13406, adult male, non-type, 113.4 mm SL, Mackay, Queensland, Australia (photograph Jon Fong).

Figure 11. 

Hippocampus procerus, AMS I.A4205, juvenile female, non-type, Point Curtis, Queensland, Australia (photograph Jeff Johnson).

Morphological remarks

In his original description, Kuiter (2001:328–329) erected H. procerus based on several observations on its distinguishing characters: “Previously confused with Hippocampus tristis and H. whitei, H. procerus is more similar to the latter, differing from it in having a taller and spinier coronet, higher fin-ray counts, and generally a spinier physiogamy.” We show that morphometric, meristic, and diagnostic morphological characters reported herein (Tables 2, 3) correspond closely among the non-type specimens of H. whitei from NSW, type and non-type specimens referred to as H. procerus from Gold Coast Seaway, Moreton Bay, Elliot Heads, Bundaberg, and Mackay, QLD, and the holotype specimen of H. procerus from Hervey Bay, QLD.

Based on the material examined, we found minor variation in coronet height in proportion to the head (45.5–46.6% in H. whitei from Nelson Bay, NSW vs. 45.1–47.8% in H. procerus from Gold Coast Harbour, QLD, 48.9–52.9% in the paratypes from Moreton Bay, QLD, 44.8% in the holotype from Hervey Bay, QLD, 50.8% in the paratype from Bundaberg, QLD and 46.7% from Mackay, QLD). The non-type specimens are comprised of juveniles, subadults, and adults, all of which exhibit distinct and tall coronets. However, we noted that in juveniles the coronet protrudes anteriad whereas in subadults and adults it is strongly angled dorsoposteriad. Similarly, dorsal fin ray counts exhibited marginal differences (17 in non-type specimens of H. whitei vs. 18 in all the specimens of H. procerus from Queensland), which may reflect north-south clinal variation. We did not observe an overall spinier physiognomy in the majority of adult specimens of H. procerus relative to H. whitei. However, a spinier physiognomy was present in one juvenile specimen from Mackay, and Port Curtis, QLD (Figs 10, 11), respectively, and one adult specimen from Burnett River (Fig. 9) and Waddy Point, QLD (Fig. 12), respectively, on all principal trunk and tail ridges and head. It has been observed that in juvenile and subadult H. whitei from NSW (<8 cm Total Length) that spines are more pronounced, but as they increase in size the spines disappear, with specimens > 12 cm TL being much smoother and spines not obvious. The adult specimens from Burnett River and Waddy Point, QLD, are an exception to these observations and appear to reflect variation in spine morphology similarly observed in juvenile H. whitei.

Figure 12. 

Hippocampus procerus, QM I.39656, adult female, non-type, Waddy Point Queensland, Australia (photograph Jeff Johnson).

We also observed across the majority of examined adult specimens the following key diagnostic morphological characters (Table 3): the absence of true neck spines between the coronet and the 1st superior trunk ring spines (small neck spines were detected in juvenile specimens; variation in neck ridge topology is often mistaken for true neck spines in adult specimens), indiscernible or small parietal spine, three cleithral ring spines with the uppermost spine at the dorsal level of the pectoral fin base, presence of a distinct snout spine, four subdorsal ridge spines (3/0,1,0), and superior trunk ridge with enlarged spines on 1st and 8th tail ridges. Based on these findings, we find that spine physiognomy, neck spines present or absent in juveniles and adults, respectively, and subtle differences in meristics, are unreliable diagnostic characters, and that key and informative morphological characters are congruent across all specimens, which conform to the diagnosis of H. whitei. Therefore, it can be concluded that the species-level classification of H. procerus is unsupported, and that H. procerus may be treated as a junior synonym of H. whitei.

Several seahorse species endemic to Australia, including Indo-Pacific seahorses with overlapping latitudinal distributions in Queensland, Australia, are superficially similar to and often misidentified as juvenile and adult H. whitei (Kuiter 2001; Table 5). These species include H. abdominalis Lesson, 1827, H. angustus Günther, 1870, H. breviceps Peters, 1869, H. dahli Ogilby 1908, H. histrix Kaup, 1856, H. jugumus Kuiter, 2001, H. kelloggi Jordan & Snyder, 1901, H. planifrons Peters, 1877, H. spinosissimus Weber, 1913, and H. zebra Whitley, 1964. Despite the morphological similarities, meristic and diagnostic morphological characters support the distinctions among these species (Table 4).

Comparison of morphological characters in H whitei from NSW and other Hippocampus spp. occurring in Australia.

H. whitei H. abdominalis H. angustus H. breviceps H. dahli H. histrix H. jugumus H. kelloggi H. planifrons H. spinosissimus H. zebra
Trunk rings 11 12–13 11 11 11 11 12 11 11 11 11
Tail rings 33–35 44–48 39–41 38–42 37–40 33–34 37 39–41 37–38 35–36 37–39
Snout stripe or striation pattern absent present
Coronet distinct, tall low distinct, tall distinct, tall low distinct, tall distinct, tall distinct, tall low distinct, tall distinct, tall
Subdorsal rings 2+1 3-5+1-2 2+1 3+1 2-3+1-2 2+1 3+2 2+1 3-4+1 2+1 2-3+1
Subdorsal ring spines 3/0,1,0 5/0,0,1,1,1 3/0,1,0 3-4/0,0,1,0 3/0,1,1 3/0,1,0 4/0,1,1,1,1 3/0,1,0 4/0,0,1,1 3/0,1,0 3-4/0,1,0
Cleithral ring discontinuous
Upper cleithral spine dorsal level of pectoral fin base ventral of gill opening dorsal level of pectoral fin base ventral of gill opening ventral of gill opening ventral of gill opening dorsal level of pectoral fin base ventral of gill opening ventral of gill opening ventral of gill opening dorsal level of pectoral fin base
Neck spine absent absent present absent absent present present absent absent present absent
Eye spine single double single
Lateral head spine single and small double and large single and small

Distribution of haplotypes based on partial mtDNA COI sequence data (655 bp) tabulated across sampled H. whitei and localities in central NSW and southern QLD.

Species designation Collection locality Nucleotide position Haplotype
Hippocampus whitei_1300a_CO1_Nelson Nelson 81 A
Hippocampus whitei_1767_CO1_GoldCoast Gold Coast 174 T
Hippocampus whitei_1783_CO1_GoldCoast Gold Coast 174 T
Hippocampus whitei_1364_CO1_Forster Forster 174 T
Hippocampus whitei_1365_CO1_Forster Forster 174 T
Hippocampus whitei_1295_CO1_Nelson Nelson 259 C
Hippocampus whitei_1364_CO1_Forster Forster 342 G
Hippocampus whitei_1365_CO1_Forster Forster 342 G
Hippocampus whitei_1767_CO1_GoldCoast Gold Coast 378 A
Hippocampus whitei_1783_CO1_GoldCoast Gold Coast 378 A
Hippocampus whitei_1364_CO1_Forste Forster 378 A
Hippocampus whitei_1365_CO1_Forster Forster 378 A
Hippocampus whitei_1305_CO1_Nelson Nelson 412 A
Hippocampus whitei_1353_CO1_Nelson Nelson 412 A
Hippocampus whitei_0418_CO1_Sydney Sydney 429 G
Hippocampus whitei_0470_CO1_Sydney Sydney 429 G
Hippocampus whitei_1767_CO1_GoldCoast Gold Coast 489 G
Hippocampus whitei_1783_CO1_GoldCoast Gold Coast 489 G
Hippocampus whitei_1364_CO1_Forster Forster 489 G
Hippocampus whitei_1365_CO1_Forster Forster 489 G
Hippocampus whitei_1295_CO1_Nelson Nelson 495 G
Hippocampus whitei_1783_CO1_GoldCoast Gold Coast 504 T
Hippocampus whitei_1364_CO1_Forster Forster 513 T

Genetic remarks

Meristic, morphometric, and key diagnostic morphological characters in our study did not support the separation of H. procerus from H. whitei into two distinct species. Here we further confirm the synonymization of H. procerus with H. whitei based on partial mitochondrial COI (655 bp) data. This analysis is based on sequences generated from 31 H. whitei individuals sampled from Empire Bay, Forster (Wallis Lake), Port Hacking, Nelson Bay, Sydney Harbour, and Tuggerah Lake, NSW, and from 4 specimens referred to as H. procerus from Southport, Gold Coast Seaway, QLD. Alignment of sequence data detected 23 variable sites without any indels, resulting in 14 haplotypes: one in Sydney, four in Nelson Bay, five in Forster, and four in Gold Coast Seaway (Suppl. material 1, 2). Three haplotypes are shared between Forster and Gold Coast Seaway whereas no other haplotypes are shared between collection localities. One unique haplotype was obtained in Sydney, four in Nelson Bay, two in Forster, and one in Gold Coast Seaway (Suppl. material 1, 2). Fig. 12 shows a neighbour-joining tree based on the same mtDNA COI data, which recovered H. procerus as paraphyletic with respect to H. whitei. Hippocampus procerus clustered among individuals of H. whitei from Forster, NSW in one subclade and with individuals from several localities in NSW in another subclade. Additionally, genetic distance analysis (uncorrected p distances) of the same data failed to discriminate H. procerus from H. whitei (Suppl. material 3), which revealed an average intraspecific divergence of 0.002%, further confirming lack of support of species status for H. procerus.

Figure 13. 

Neighbor-joining tree based on mtDNA COI sequences showing the relationships among specimens of H. whitei collected from various sites in NSW and H. procerus from Southport, Gold Coast Harbour, QLD. Numbers in branches indicate bootstrap probabilities obtained from 1000 bootstrap replications. Scale bar = genetic distance of 0.02.

Distribution and habitat

Hippocampus whitei is known to occur in coastal estuaries and embayments of central NSW and southern QLD, Australia. In central NSW it has been recorded, from south to north, in St. Georges Basin, Port Hacking, Botany Bay, Sydney Harbour, Hawkesbury River, Tuggerah Lake, Lake Macquarie, Port Stephens, Wallis Lake – Forster, and Tweed River. The record from St Georges Basin was based on a recent sighting and photograph of a small juvenile in January 2018 that was logged through REDMAP (http://www.redmap.org.au/sightings/3379/) and therefore extends the range reported by Harasti et al. (2012) southwards by 70 km. A previous 1903 Australian Museum record from Lake Illawarra cannot be confirmed as the locality information is likely erroneous (Mark McGrouther, pers. comm.) and whilst it is possible that H. whitei could occur in Lake Illawarra, at this stage there is no definitive evidence. Museum records indicate the species has been recorded in QLD within the Gold Coast Seaway, at various locations around Moreton Bay estuary, Hervey Bay, Waddy Point, Elliot Heads, Bundaberg, Port Curtis, and Mackay. The synonymization of H. procerus extends the northward range significantly by approximately 1,000 kilometres for H. whitei to Mackay QLD; as of now, this is the most northern location with confirmed H. whitei specimens. However, its current occurrence in the Mackay region, Port Curtis, Burnett River, and Bundaberg, is unknown as it has not been recorded in those locales since 1939, 1929, and 1938, respectively. The most recent northern records are from Elliot Heads in 1982 and Waddy Point in 2005.

Additionally, museum records claim species occurrences of H. whitei outside its geographic range, in South Australia, Victoria Australia, Papua New Guinea, South Africa, Solomon Islands, and Vanuatu (Kuiter 2009; Lourie et al. 2016). However, these specimens have subsequently been re-identified by the authors as H. breviceps, H. camelopardalis, H. kelloggi, or H. spinosissimus (see Table 6). The specimens originally identified as H. whitei from Port Moresby, Papua New Guinea and the Solomon Islands are no longer accessible and therefore cannot be re-identified; however, we consider them highly unlikely to be H. whitei since it is markedly outside the range for this species. We now consider that the species is constrained to estuaries and embayments along the east coast of Australia from Hervey Bay, QLD, in the north to St Georges Basin, NSW, in the south.

List of seahorse specimens originally identified as H. whitei, including voucher number, collection date, collection location, and status.

Original identification Voucher number Collection date Collection location Species
H. whitei AMS I.6637 1885 Port Moresby, Papua New Guinea Hippocampus sp.
SU 35442 1912 Corny Point, South Australia H. breviceps
AMS IA4205 1929 Port Curtis, Qld, Australia H. spinosissimus
CAS-SU 31443 1934 Durban Bay, KwaZulu-Natal, South Africa H. camelopardalis
MNHN-IC-2008-1326 2006 Espiritu Santo, Vanuatu H. kelloggi
MNHN-IC-2008-1441 2006 Espiritu Santo, Vanuatu H. kelloggi
MNHN-IC-2008-1662 2006 Malekula, Vanuatu H. kelloggi
MCZ 168083 unknown Western Port, Victoria, Australia H. breviceps

Hippocampus whitei occurs in a variety of habitats including seagrasses, soft corals, sponge gardens and artificial structures to depths of 12 m (Hellyer et al. 2011; Harasti et al. 2014a; Manning et al. 2018), and is known to display strong site fidelity and monogamous behaviour (Vincent and Sadler 1995; Vincent et al. 2005; Harasti and Gladstone 2013). The locations with the largest recorded populations are found within Sydney Harbour and Port Stephens (Harasti et al. 2012; Harasti et al. 2014b), beyond which there is very little information about the occurrence, habitat use, and population numbers in QLD as the species is not known to be regularly found in any QLD locations and is seldom seen or collected.

We introduced this paper with a quote from John White (1736–1832) who was under the assumption that the Mediterranean and North Atlantic seahorse H. hippocampus and H. whitei from Australia were conspecific due to highly similar morphology. Seahorse taxonomy has been in a state of confusion since its inception. While comprehensive revisions of the genus have greatly advanced our understanding of how many species of seahorses exist (Lourie et al. 2016), much further work remains to answer this most fundamental question about one of the world’s most extraordinary fish.

Video 1. 

Hippocampus whitei, in situ, Seahorse Gardens, Nelson Bay, NSW, Australia (video by David Harasti 2011).

Acknowledgements

We are grateful to: Jeff Leis, Senior Fellow, Ichthyology Collection, Australian Museum, for discussions on H. whitei; Jeff Johnson, Collection Manager, Ichthyology, Biodiversity Program, Queensland Museum, for discussions on and providing an image of a paratype of H. whitei from Queensland; Amanda Hay, Mark McGrouther, and Matthew Lockett, Department of Ichthyology, Australian Museum, for curatorial assistance; Jon Fong and David Catania, Ichthyology, California Academy of Sciences, for curatorial assistance and images of paratypes and non-type specimens of H. procerus; Kerryn Parkinson, Technical Officer, Ichthyology and Institute Data and DigiVol Coordinator, Digital Collections and Citizen Science, Australian Museum Research Institute, for an image of the holotype of H. procerus; and Beth Tate and Brian Simison of the Center for Comparative Genomics at the California Academy of Sciences for support with generating genetic data. This work was partially funded by a grant to DH from the Sydney Aquarium Conservation Fund.

References

  • Bleeker P (1855) Over eenige visschen van Van Diemensland. Verhandelingen van het Koninklijke Akademie van Wetenschappen te Amsterdam 2: 17, 28–31.
  • Bruckner AW, Field JD, Daves N (2005) Proceedings of the International Workshop on CITES Implementation for Seahorse Conservation and Trade, February 3–5, 2004, Mazatlan, Sinaloa, Mexico.
  • Hamilton H, Saarman N, Short G, Sellas AB, Moore B, Hoang T, Grace CL, Gomon M, Crow K, Simison WB (2017) Molecular phylogeny and patterns of diversification in Syngnathid fishes. Molecular phylogenetics and Evolution 107: 388–403. https://doi.org/10.1016/j.ympev.2016.10.003
  • Han S, Kim JK, Kai Y, Seno H (2017) Seahorses of the Hippocampus coronatus complex: taxonomic revision, and description of Hippocampus haema, a new species from Korea and Japan (Teleostei, Syngnathidae). ZooKeys 712: 113–139. https://doi.org/10.3897/zookeys.712.14955
  • Harasti D, Martin‐Smith K, Gladstone W (2012) Population dynamics and life history of a geographically restricted seahorse, Hippocampus whitei. Journal of Fish Biology 81(4): 1297–1314. https://doi.org/10.1111/j.1095-8649.2012.03406.x
  • Harasti D, Glasby TM, Martin-Smith KM (2010) Striking a balance between retaining populations of protected seahorses and maintaining swimming nets. Aquatic Conservation: Marine and Freshwater Ecosystems 20(2): 159–166. https://doi.org/10.1002/aqc.1066
  • Harasti D, Gladstone W (2013) Does underwater flash photography affect the behaviour, movement and site persistence of seahorses? Journal of Fish Biology 83: 1344–1353. https://doi.org/10.1111/jfb.12237
  • Harasti D, Martin-Smith K, Gladstone W (2014a) Ontogenetic and sex-based differences in habitat preferences and site fidelity of the White’s seahorse Hippocampus whitei. Journal of Fish Biology 85: 1413–1428. https://doi.org/10.1111/jfb.12237
  • Harasti D (2016) Declining seahorse populations linked to loss of essential marine habitats. Marine Ecology Progress Series 546: 173–181. https://doi.org/10.3354/meps11619
  • Hellyer CB, Harasti D, Poore AG (2011) Manipulating artificial habitats to benefit seahorses in Sydney Harbour, Australia. Aquatic Conservation: Marine and Freshwater Ecosystems 21(6): 582–589. https://doi.org/10.1002/aqc.1217
  • Kuiter RH (2001) Revision of the Australian seahorses of the genus Hippocampus (Syngnathiformes: Syngnathidae) with descriptions of nine new species. Records-Australian Museum 53(3): 293–340. https://doi.org/10.3853/j.0067-1975.53.2001.1350
  • Lourie SA, Pollom RA, Foster SJ (2016) A global revision of the Seahorses Hippocampus Rafinesque 1810 (Actinopterygii: Syngnathiformes): Taxonomy and biogeography with recommendations for further research. Zootaxa 4146(1): 1–66. https://doi.org/10.11646/zootaxa.4146.1.1
  • Short G, Smith R, Motomura H, Harasti D, Hamilton H (2018) Hippocampus japapigu, a new species of pygmy seahorse from Japan, with a redescription of H. pontohi (Teleostei, Syngnathidae). ZooKeys 779: 27–49. https://doi.org/10.3897/zookeys.779.24799
  • Steindachner F (1866) Zur Fischfauna von Port Jackson of Australien. Sitzungberichte Akademie Wissenschaften, Wien 53: 424–480.
  • Vincent AC, Evans KL, Marsden AD (2005) Home range behaviour of the monogamous Australian seahorse, Hippocampus whitei. Environmental Biology of Fishes 72(1): 1–12. https://doi.org/10.1007/s10641-004-4192-7