Recognition and Distribution of Two North Atlantic Gadiculus Species, G
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fishes Article Recognition and Distribution of Two North Atlantic Gadiculus Species, G. argenteus and G. thori (Gadidae), Based on Otolith Morphology, Larval Pigmentation, Molecular Evidence, Morphometrics and Meristics Pieter A. M. Gaemers 1,* and Jan Y. Poulsen 2 ID 1 Joost van den Vondelstraat 30, Winterswijk 7103 XW, The Netherlands 2 Department of Fish and Shellfish, Pinngortitaleriffik (Greenland Institute of Natural Resources), Kivioq 2, Post Box 570, Nuuk 3900, Greenland; [email protected] * Correspondence: [email protected]; Tel.: +31-543-750-383 Academic Editor: Maria Angeles Esteban Received: 28 July 2017; Accepted: 3 August 2017; Published: 29 August 2017 Abstract: The silvery pout genus Gadiculus consists of small aberrant codfishes with several extinct and currently only one recognized extant species. The oldest representatives of a Gadiculus lineage known from otoliths are Early Miocene in age. Fossil evidence has showed Gadiculus to originate from older genera diverging early from other true cods of the family Gadidae. As adult specimens of different species have been found to be highly similar and difficult to distinguish based on meristic and morphometric data, the number of species in this gadid genus has been controversial since different larval morphotypes were first discovered some 100 years ago. For almost 70 years, Gadiculus thori and Gadiculus argenteus have been considered subspecies only, with a distribution in the Northeast Atlantic Ocean including the Mediterranean. In this study, we resolve the long-standing issue of extant Gadiculus not being monotypic. New results in the form of distinct adult otoliths and molecular data unambiguously show two species of Gadiculus present—in agreement with larval morphotypes. Morphometric, meristic and molecular characters, as well as larval pigmentation are discussed in addition to present and past geographic distributions of the two taxa from distributions of fossil otoliths. At present, the cold-water species Gadiculus thori (northern silvery pout) is distributed in cold-temperate and subarctic latitudes in the Northeast Atlantic, including a new range extension off Southeast Greenland. Gadiculus argenteus (southern silvery pout) occurs in warmer waters and is distributed in the warm-temperate East Atlantic and Mediterranean. Fossil otoliths show that both species often co-existed in the Mediterranean from the Late Pliocene to the Middle Pleistocene. Keywords: taxonomic revision; otolith; Cox1 barcode; larval melanophore pattern; morphometrics; meristics; (palaeo)geographic distribution; Gadidae classification 1. Introduction Silvery pouts of the genus Gadiculus are the smallest extant cods in the family Gadidae. Only one species, Gadiculus argenteus (Guichenot 1850), is currently recognized with a second species described Gadiculus thori (Schmidt 1913) currently considered a synonym [1]. Most gadid species are economically important, although silvery pouts have limited commercial value due to their small size and predominantly artisanal use in some Mediterranean countries. This becomes evident considering the relatively limited number of studies present on these fishes compared to other, larger gadids. However, Gadiculus have high regional abundances and have been identified as important forage Fishes 2017, 2, 15; doi:10.3390/fishes2030015 www.mdpi.com/journal/fishes Fishes 2017, 2, 15 2 of 24 prey in trophic ecosystem dynamics [2]. Juveniles and adults of Gadiculus feed almost exclusively on various groups of pelagic crustaceans, but also eat small fish [3–6]. Gadiculus fishes are meso- to bathypelagic and show gregariousness, forming large schools in the deeper parts of the shelf and above the continental slope—usually at depths between 100 and 1000 m. However, some differences have been reported concerning depth distributions between northern Fishes 2017, 2, 15 2 of 25 and southern populations, with the former mainly between 125 and 400 m [6] and the latter mainly betweenprey 200 in and trophic 400–500 ecosystem m [ 7dynamics]. Their occurrence[2]. Juveniles and in the adults colder, of Gadiculus deeper feed waters almost in exclusively the more on southern Atlanticvarious waters groups and in of the pelagic Mediterranean crustaceans, but is likely also eat an small overlooked fish [3–6]. factor concerning depth distributions. The youngerGadiculus stages offishesGadiculus are meso-fishes to bathypelagic are known and to inhabit show gregariousness, relatively shallow forming depths. large schoolsGadiculus in fishes the deeper parts of the shelf and above the continental slope—usually at depths between 100 and have currently1000 m. However, been observed some differences in the northeastern have been reported Atlantic concerning from off depth the North distributions Capeof between Norway and the westernnorthern part and of southern the Barents populations, Sea [8 with] southwards the former mainly to Morocco, between including 125 and 400 the m [6] western and the latter and central Mediterraneanmainly between [9]. Observations 200 and 400–500 are m also [7]. presentTheir occurrence from the in Adriaticthe colder, Sea deeper [10 ],waters the entire in the Aegeanmore Sea, Thraciansouthern Sea [11 Atlantic], off the waters Turkish and in coast the Mediterranean [12], off the Syrianis likely coastan overlooked [13], and factor off theconcerning coast ofdepth Israel [14]. However,distributions. no records The from younger the tropicalstages of orGadiculus north-western fishes are known Atlantic to inhabit have ever relatively been shallow reported. depths. Gadiculus fishes have currently been observed in the northeastern Atlantic from off the North Cape Guichenot [15] (1850) described Gadiculus argenteus from the Mediterranean coast of Algiers of Norway and the western part of the Barents Sea [8] southwards to Morocco, including the western erectingand the central new Mediterranean genus Gadiculus [9]. .Observations The establishment are also present of the from genus the Adriatic was justified Sea [10], duethe entire to its large eye/bodyAegean ratio Sea, compared Thracian Sea to other[11], off gadids, the Turkish i.e., coast the eye[12], diameteroff the Syrian is coast longer [13], than and theoff the snout, coast althoughof less thanIsrael 40% [14]. head However, length. no records In addition, from theGadiculus tropical or north-westernshows a unique Atlantic oblique have ever mouth been reported. that is angled steeply upwards.Guichenot Other [15] distinguishing (1850) described characteristics Gadiculus argenteus of Gadiculus from the Mediterraneanare the large deciduouscoast of Algiers scales and the sensoryerecting canals the new with genus seven Gadiculus large. open The establishment pits (mucous of cavities)the genus on was the justified dorsal due margin to its oflarge the head eye/body ratio compared to other gadids, i.e., the eye diameter is longer than the snout, although less (Svetovidov) [16]. Subsequently, Schmidt [17] described Gadiculus thori from the North Atlantic Ocean than 40% head length. In addition, Gadiculus shows a unique oblique mouth that is angled steeply based onupwards. the following Other distinguishing characteristics: characteristics of Gadiculus are the large deciduous scales and the sensory canals with seven large open pits (mucous cavities) on the dorsal margin of the head • Different(Svetovidov) melanophore [16]. Subsequently, patterns inSchmidt post-larvae [17] described of the twoGadiculus species. thori The from post-larvae the North ofAtlanticG. argenteus showOcean three based transverse on the following pigmented characteristics: bars, whereas G. thori only exhibit one (Figure1). • At the sameDifferent stage melanophore of development, patterns in the post-larvae post-larvae of the of twoG. species. thori are, The in post-larvae general, largerof G. argenteus than those of G. argenteusshow three(Figure transverse1). pigmented bars, whereas G. thori only exhibit one (Figure 1). • Atthe At same the same stage stage of of development, development, the the post-larvae post-larvae of G. thori of G. are, thori in general,are slenderlarger than compared those of with G. argenteusG. argenteus, which (Figure are stouter 1). and shorter (Figure1). At the same stage of development, the post-larvae of G. thori are slender compared with G. • Differentargenteus number, which of vertebrae are stouter in and the shorter two species. (Figure Schmidt1). found that G. thori has 41–43 (usually 42), whereas DifferentG. argenteus numberhas of vertebrae 39–41 (usually in the two 40). species. Schmidt found that G. thori has 41–43 (usually • Geographic42), whereas distribution. G. argenteus The has number 39–41 (usually of G. thori40). specimens declines drastically from Ireland in the NorthGeographic to the Frenchdistribution. Atlantic The number coast. of Conversely, G. thori specimensG. argenteus declines occursdrastically in from increasing Ireland numbersin the North to the French Atlantic coast. Conversely, G. argenteus occurs in increasing numbers going south from the mouth of the river Gironde along the Atlantic east coast. going south from the mouth of the river Gironde along the Atlantic east coast. Figure 1. Illustrations of Gadiculus post-larvae at the same stage of development by Schmidt [17]. Figure 1. Illustrations of Gadiculus post-larvae at the same stage of development by Schmidt [17]. (A). (A). Gadiculus argenteus;(B). Gadiculus thori. The post-larvae were originally used to distinguish two Gadiculus argenteus; (B). Gadiculus