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Niche partitioning and morphospace in early stages of two sympatric Diogenichthys species (Myctophidae)

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Journal of Fish Biology
Authors:
Francisca Andrea Zavala-Muñoz at Independent
Francisca Andrea Zavala-Muñoz
  • Independent
Javier Vera-Duarte at Universidad Católica de la Santísima Concepción
Javier Vera-Duarte
Claudia A. Bustos at University of Valparaíso
Claudia A. Bustos
Jorge Angulo Aros at Instituto de Fomento Pesquero (IFOP)
Jorge Angulo Aros
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Abstract and Figures

Diet and morphospace of larval stages of two sympatric lanternfish Diogenichthys atlanticus and D. laternatus from the south‐east Pacific Ocean were compared and the covariance between both variables was assessed for each species. Diogenichthys atlanticus stomach contents consisted mainly of copepod nauplii and digested remains and this species had a broader niche than D. laternatus, in which stomach contents were highly digested. No dietary overlap was found between both species. The covariance between skull shape and diet for D. atlanticus was given by a wider mouth gape related to the presence of copepod nauplii, whilst for D. laternatus, a shorter snout and posteriorly displaced eye were related to the presence of highly digested stomach contents. Interspecific differences between diets and skull shapes suggest that both species may have undergone morphological or niche divergence to avoid competition, such as feeding at different hours or depth stratification.
Study area, in south‐east Pacific Ocean, showing the location of the oceanographic surveys to sample larval Diogenichthys spp. carried out during March–May 2015 (), September–October 2015 () and September–October 2016 ()
Study area, in south‐east Pacific Ocean, showing the location of the oceanographic surveys to sample larval Diogenichthys spp. carried out during March–May 2015 (), September–October 2015 () and September–October 2016 ()
… 
Stained and cleared heads of lanternfish postlarvae, with their landmark (LM) configuration, (a) Diogenichthys atlanticus, 11.99 mm standard length (LS); (b) D. laternatus, 10.17 mm LS. LM 1, anteriormost limit of the premaxilla; LM 2, posteriormost limit of the ethmoid cartilage in conjunction with the parasphenoid bone; LM 3, dorsal and anteriormost limit of the hyoid; LM 4, ventral margin of the angular; LM 5, anteriormost limit of the dentary; LM 6, posteriormost limit of the maxillary
Stained and cleared heads of lanternfish postlarvae, with their landmark (LM) configuration, (a) Diogenichthys atlanticus, 11.99 mm standard length (LS); (b) D. laternatus, 10.17 mm LS. LM 1, anteriormost limit of the premaxilla; LM 2, posteriormost limit of the ethmoid cartilage in conjunction with the parasphenoid bone; LM 3, dorsal and anteriormost limit of the hyoid; LM 4, ventral margin of the angular; LM 5, anteriormost limit of the dentary; LM 6, posteriormost limit of the maxillary
… 
Standard length (LS)‐frequency distribution of larval lanternfish Diogenichthys atlanticus () and D. laternatus () examined in this study
Standard length (LS)‐frequency distribution of larval lanternfish Diogenichthys atlanticus () and D. laternatus () examined in this study
… 
(a) Feeding incidence (%OI) during a virtual day for larval Diogenichthys atlanticus and (b) larval D. laternatus (the numbers of larvae analysed by hour are shown in parentheses). (c) The total prey volume per gut (TVPG) during a virtual day for larval Diogenichthys atlanticus and (d) larval D. laternatus. (e) Percentage of prey remains (digested remains + chitinous remains) during a virtual day. , Hours of darkness. () D. atlanticus, () D. laternatus
(a) Feeding incidence (%OI) during a virtual day for larval Diogenichthys atlanticus and (b) larval D. laternatus (the numbers of larvae analysed by hour are shown in parentheses). (c) The total prey volume per gut (TVPG) during a virtual day for larval Diogenichthys atlanticus and (d) larval D. laternatus. (e) Percentage of prey remains (digested remains + chitinous remains) during a virtual day. , Hours of darkness. () D. atlanticus, () D. laternatus
… 
Discriminant function analysis (DFA) comparing frequency distribution of the skull morphospace of larval Diogenichthys atlanticus (DA; ) and D. laternatus (DL; ). Wireframe graphs indicate the mode of the shape configuration for each species. The scale of the wireframe was −2 for D. atlanticus () and 1.8 for D. laternatus (). Grey wireframes correspond to the consensus shape (scale = 0)
+2
Discriminant function analysis (DFA) comparing frequency distribution of the skull morphospace of larval Diogenichthys atlanticus (DA; ) and D. laternatus (DL; ). Wireframe graphs indicate the mode of the shape configuration for each species. The scale of the wireframe was −2 for D. atlanticus () and 1.8 for D. laternatus (). Grey wireframes correspond to the consensus shape (scale = 0)
… 
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REGULAR PAPER
Niche partitioning and morphospace in early stages of two
sympatric Diogenichthys species (Myctophidae)
Francisca Zavala-Muñoz
1
| Javier Vera-Duarte
1
| Claudia A. Bustos
1,3
|
Jorge Angulo-Aros
2
| Mauricio F. Landaeta
1,3,4
1
Laboratorio de Ictioplancton (LABITI), Escuela
de Biología Marina, Facultad de Ciencias del
Mar y de Recursos Naturales, Universidad de
Valparaíso, Viña del Mar, Chile
2
Departamento de Oceanografía y Medio
Ambiente, Instituto de Fomento Pesquero,
Valparaíso, Chile
3
Centro de Observación Marino para Estudios
de Riesgos del Ambiente Costero (COSTA-R),
Universidad de Valparaíso, Viña del Mar, Chile
4
Fundación Ictiológica, Santiago, Chile
Correspondence
Mauricio F. Landaeta, Laboratorio de
Ictioplancton (LABITI), Escuela de Biología
Marina, Facultad de Ciencias del Mar y de
Recursos Naturales, Universidad de Valparaíso,
Avenida Borgoño 16344, Reñaca, Viña del
Mar, Chile.
Email: landaeta.mauricio@gmail.com
Funding information
This study was funded by Comite
Oceanografico Nacional de Chile (CONA),
through projects CIMAR 21-I 15-05 and
CIMAR 22-I 16-02, adjudicated to MFL and
CAB and by the Economy Undersecretary
project ASIPA 2016-23 to Instituto de
Fomento Pesquero.
Abstract
Diet and morphospace of larval stages of two sympatric lanternfish Diogenichthys
atlanticus and D. laternatus from the south-east Pacific Ocean were compared and
the covariance between both variables was assessed for each species. Diogenichthys
atlanticus stomach contents consisted mainly of copepod nauplii and digested
remains and this species had a broader niche than D. laternatus, in which stomach
contents were highly digested. No dietary overlap was found between both species.
The covariance between skull shape and diet for D. atlanticus was given by a wider
mouth gape related to the presence of copepod nauplii, whilst for D. laternatus,a
shorter snout and posteriorly displaced eye were related to the presence of highly
digested stomach contents. Interspecific differences between diets and skull shapes
suggest that both species may have undergone morphological or niche divergence to
avoid competition, such as feeding at different hours or depth stratification.
KEYWORDS
Chile, diet, feeding, geometric morphometrics, mouth gape, post-larva, South Pacific Ocean
1|INTRODUCTION
Lanternfishes (Teleostei, Myctophidae) are one of the most diverse and
numerous groups of deep-sea fishes endemic to open-ocean environ-
ments. A number of molecular studies and revisions in recent years
have assessed the diversity of Myctophidae, but there is yet no consen-
sus about the number of species (c. 250), genera (33–39) and subfam-
ilies (2–5) contained in this group (Denton, 2014; Fricke et al., 2019;
Martin et al., 2018; Mirande, 2016). Most of the species inhabit the
mesopelagic (200–1000 m depth) and bathypelagic (1000–4000 m)
zones, where no downwelling sunlight penetrates. They exhibit exten-
sive diel vertical migrations toward the surface at night in order to feed,
mostly on copepods (Baird et al., 1975; Kinzer & Schulz, 1985),
although some species may show different patterns of vertical distri-
bution: semi-migrants, passive migrants and non-migrants (Watanabe
et al., 1999). Because of this vertical distribution, myctophids play an
important ecological role as a trophic link between primary and ter-
tiary consumers and in vertical carbon fluxes in oceans worldwide
(Conley & Hopkins, 2004; Rodríguez-Graña et al., 2005). Adult
morphospace spans from dorsoventrally compressed and caudally
elongated to lobate body shape (Denton & Adams, 2015), exhibiting
broad plasticity in the eye and mouth size, independent of their depth
distribution (de Busserolles et al., 2013; Martin & Davis, 2016).
Contrary to most adults, larval stages of myctophids are distrib-
uted in the upper 200 m of depth, feeding on zooplankton near the
surface during the day and migrating to deeper waters during the
night (Loeb, 1979; Sassa et al., 2001). Also, there is a wide spectrum
Received: 26 April 2019 Accepted: 26 August 2019
DOI: 10.1111/jfb.14128
FISH
J Fish Biol. 2019;95:1275–1285. wileyonlinelibrary.com/journal/jfb © 2019 The Fisheries Society of the British Isles 1275
... Feeding ecology studies on fish larvae and juveniles are scarce (Nunn et al., 2012). Regarding myctophids, investigations on larval feeding ecology were conducted in many different oceanographic regions such Central Atlantic (Conley and Hopkins, 2004), Pacific (Sassa and Kawaguchi, 2005;Rodríguez-Graña et al., 2005;Sassa, 2010, Zavala-Muños, 2019, Western Mediterranean (Bernal et al., 2013;Bernal et al., 2020;Contreras et al., 2015), Southern Ocean (Nirazuka et al., 2021) and Southwest Atlantic Ocean, where only one recent study (Contreras et al., 2019) contributed to reduce this relevant knowledge gap. ...
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Myctophids are central in ocean food webs, yet knowledge of the ecology of larval stages is sparse. We investigated if larval feeding ecology is different in continental shelf break waters compared to waters off oceanic islands in the western Tropical Atlantic. The larvae were collected through diurnal and nocturnal oblique hauls using a Bongo net and stomach contents were analyzed. The larvae ranged between 2.27 and 16.5 mm in standard length. Diet composition was different in the slope and islands (Permutational Multivariate Analysis of Variance (PERMANOVA), P < 0.001). Diatoms (mainly Thalassiosira spp. and fragments of diatoms) were numerically important in the diet at the slope site (69% of relative importance). Copepods were the most relevant prey (71% of relative importance) near the islands. Copepods were the biomass-dominant dietary item at both areas, alongside ostracods near the islands. Smaller prey items were more important for smaller larvae, particularly those measuring up to 4 mm. Larger prey became relatively more important as the larvae grew to at least 8 mm. Larvae fed mostly during the daytime regardless of their size class.
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... Recent studies have reported high morphofunctional variability in myctophid body and otolith shape (Tuset et al., 2018), jaw size (Martin & Davis, 2016) and dentition (Martin & Davis, 2020). Coupled with evidence of low overlap in the diet of sympatric species (Zavala-Munoz et al., 2019), these studies also suggest that co-existing lanternfishes can undergo niche differentiation by adapting morphologically and behaviourally to their environment. Obtaining comprehensive data on species traits, bioluminescent signal properties, vertical distributions and ecological niche characteristics might require the development of methods to observe midwater species behaviour, and the use of contemporary genomic techniques for dietary analysis, or for detection of species via environmental DNA. ...
Global phylogeography of hyperdiverse lanternfishes indicates sympatric speciation in the deep sea
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Aim Lanternfishes (Myctophidae) are one of the most species‐rich families of mid‐water fishes. They inhabit the mesopelagic zone, where physical barriers to dispersal and gene flow are permeable. Thus, modes of speciation that rely exclusively on geographical separation are potentially of less importance than those that rely more prominently on evolution of assortative mating through divergent habitat use and/or sexual signals, including visual signals from bioluminescent light organs. Here we used phylogenetic, ecological and morphological data to investigate the roles of geography, habitat use and lateral photophores in lanternfish speciation. Location Global. Time period Data collected between 1950 and 2015. Major taxa studied Lanternfishes (Myctophidae). Methods Ecological niche models (ENMs) were developed for 167 species, enabling the community composition of 33 mesopelagic ecoregions to be determined. Sequence data for seven protein‐coding regions from 175 species were used to reconstruct a phylogenetic tree of Myctophidae. Age‐overlap correlation tests were conducted using this phylogeny with outputs from ENMs (pairwise geographical overlap and pairwise ecological niche overlap, n = 136), in addition to matrices of pairwise depth overlap ( n = 158) and photophore pattern dissimilarity ( n = 161). Results Communities assembled according to nine broad climatic regions, and recently diverged species pairs possessed greater geographical and ecological niche overlap than more distantly related species, indicating that sympatric or parapatric speciation might be dominant modes of divergence. Differences in photophore patterns increased with the relative age of speciation events, suggesting that photophore patterns are largely constrained by phylogeny. Main conclusions Based on this evidence, we suggest that large‐scale oceanographic features structure the diversity of lanternfish communities and that speciation within this family of deep‐water fishes might not have required geographical isolation.
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... High diversity in fish assemblages is often accompanied by high rates of resource or niche partitioning (Ross 1986;Willis et al. 2005;Ye et al. 2013;Comte et al. 2016). For larval fish, niche partitioning may occur through trophic partitioning during ontogenetic development (Stoffels and Humphries 2003;Nunn et al. 2007;Llopiz and Cowen 2009), differences in morphology (e.g., Zavala-Muñoz et al. 2019), and habitat utilisation (e.g., George and Hadley 1979;Floyd et al. 1984), or indirectly through variation in spawning phenologies and spawning habitats among species (Kramer 1978;Floyd et al. 1984;Grabowski and Isely 2007;Krabbenhoft et al. 2014). However, the specific habitat (e.g., structural complexity, temperature), hydrological (e.g., high or low flows), and resource (e.g., food) drivers of variation in diversity of larval riverine fish over space and time remain poorly understood. ...
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Several hypotheses and conceptual models propose to explain mechanisms mediating riverine fish abundance, but few empirical studies to date have explored their utility in tropical systems. This study assesses key components of previous fish recruitment models by exploring spatiotemporal variation in larval fish assemblages in response to predicted key drivers in a tropical Australian river catchment. Data on larval fish composition and abundance, alongside hydrological, hydraulic, habitat and food variables, were collected monthly to bimonthly over one year at eight sites. Variables which best predicted larval fish abundance and diversity were determined with Boosted Regression Trees. The most commonly important predictors were microfauna abundance, structural habitat complexity and temperature, with high values of each predicting high larval fish abundance and diversity. Maximum larval diversity occurred when discharge was highest because several wet-season spawning taxa occurred alongside aseasonally spawning taxa. These findings support previous generic fish recruitment models, demonstrating the utility of their inclusion in the recent Riverine Recruitment Synthesis Model and the applicability of this model for describing processes important for tropical riverine fish recruitment.
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... For example, this method showed that the larvae of Gobiesox marmoratus, a rocky reef species, had less robust and more hydrodynamic bodies when they carried ectoparasitic copepods (Jahnsen-Guzmán et al., 2018). These morphological changes in marine larval fishes have been related to different hydrographic and biological characteristics, such as wind stress and coastal upwelling , temperature (Galeano-Chavarria et al., 2020;Landaeta et al., 2019), or to changes in preferential prey during each larval stage (Bernal-Durán & Landaeta, 2017;Galeano-Chavarria et al., 2020;Landaeta et al., 2019;Zavala-Muñoz et al., 2019). In addition, these characteristics might induce considerable differences in body proportions associated with the increase in fish larval size (Osse & Van den Boogaart, 1995;van Snik et al., 1997), a phenomenon that is known as allometry (Fuiman, 1983). ...
Influence of oceanographic conditions on the body shape variability of Scomber japonicus larvae from the western coast of the Baja California Peninsula
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  • Jan 2022
Pacific chub mackerel (Scomber japonicus) is a relevant fishery resource shared among three countries in the northeastern Pacific. The spatiotemporal distribution of larvae has been related to the convergence of oceanographic mesoscale structures, which can generate considerable variability in the morphology of fish larvae. The main goal of this work was to describe the shape changes of larval S. japonicus and their relationship with oceanographic variability, through geometric morphometric analysis to assess the seasonal variability of 10 homologous landmarks distributed on the pre‐anal section of 331 larvae from off the western coast of the Baja California Peninsula (WCBCP), Mexico (2006–2008). The results showed two principal morphotypes in Pacific chub mackerel larvae: The first morphotype had a more hydrodynamic body (longer and shallower head), influenced by increased sea surface flow and colder sea surface temperatures mainly during spring, and the second morphotype had robust larvae (shorter and deeper head) under slower current flow and warmer sea surface temperatures during winter and summer. We concluded that changes in larval body shape are influenced mainly by sea surface flow and sea temperatures, probably associated with the ability to reach higher swimming speeds during feeding success.
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... These previous works offer an insight into lanternfish speciation and provoke new questions, inspiring a need for deeper understanding of diversification in this abundant and diverse group. Few studies have explored the anatomical variation associated with lanternfish feeding (e.g., Alwis & Gjøsaeter, 1988;Martin & Davis, 2016;Zavala-Muñoz, Vera-Duarte, Bustos, Angulo-Aros, & Landaeta, 2019). Martin and Davis (2016) identified considerable variation in the size of the jaws of lanternfishes, concluding that the subfamily Myctophinae possessed generally shorter jaws with significant jaw elongation in taxa within the subfamilies Lampanyctinae and Notolynchinae. ...
The evolution of specialized dentition in the deep-sea lanternfishes (Myctophiformes)
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  • J MORPHOL
The evolution of heterodonty, the possession of varied tooth morphologies on the jaws of animals, has been relatively unexplored in ray‐finned fishes compared to terrestrial vertebrates, and to an even lesser degree in deep‐sea fish lineages. Lanternfishes (Myctophiformes) are an abundant and species‐rich group endemic to deep‐sea pelagic habitats. In this study, we document the presence of heterodonty on the oral jaws of lanternfishes, identifying differing anatomical and positional variations of dentition. We survey the anatomical variation in tooth morphology on the oral jaws of 114 lanternfish species across 37 genera and integrate our findings with a hypothesis of evolutionary relationships of lanternfishes to infer the number of times heterodonty evolved in this lineage. Our results indicate that heterodonty evolved at least six separate times on the oral jaws of lanternfishes, occurring as variable tooth morphologies in combination with villiform teeth. These combinations of tooth types include villiform plus hooked teeth, villiform plus hooked and recurved teeth, villiform plus spade, tricuspid, and hooked teeth, and villiform plus caniniform teeth. The reoccurring evolution of hooked teeth on the premaxilla and dentary in lanternfishes suggests heterodonty may serve an important functional role in their pelagic deep‐sea environment. Hooked teeth could aid in securing and retaining prey in the oral cavity and allow for species to specialize on differing food resources, vital attributes for organisms living in open‐ocean habitats.
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Morphospace of lanternfish larvae and their interplay with oceanographic conditions from the southeastern Pacific Ocean
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Eschmeyer's catalog of fishes: Genera, species, references.
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Available online under http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
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Article
  • Jan 2018
Massive parallel sequencing allows scientists to gather DNA sequences composed of millions of base pairs that can be combined into large datasets and analyzed to infer organismal relationships at a genome-wide scale in non-model organisms. Although the use of these large datasets is becoming more widespread, little to no work has been done in estimating phylogenetic relationships using UCEs in deep-sea fishes. Among deep-sea animals, the 257 species of lanternfishes (Myctophiformes) are among the most important open-ocean lineages, representing half of all mesopelagic vertebrate biomass. With this relative abundance, they are key members of the midwater food web where they feed on smaller invertebrates and fishes in addition to being a primary prey item for other open-ocean animals. Understanding the evolution and relationships of midwater organisms generally, and this dominant group of fishes in particular, is necessary for understanding and preserving the underexplored deep-sea ecosystem. Despite substantial congruence in the evolutionary relationships among deep-sea lanternfishes at higher classification levels in previous studies, the relationships among tribes, genera, and species within Myctophidae often conflict across phylogenetic studies or lack resolution and support. Herein we provide the first genome-scale phylogenetic analysis of lanternfishes, and we integrate these data from across the nuclear genome with additional protein-coding gene sequences and morphological data to further test evolutionary relationships among lanternfishes. Our phylogenetic hypotheses of relationships among lanternfishes are entirely congruent across a diversity of analyses that vary in methods, taxonomic sampling, and data analyzed. Within the Myctophiformes, the Neoscopelidae is inferred to be monophyletic and sister to a monophyletic Myctophidae. The current classification of lanternfishes is incongruent with our phylogenetic tree, so we recommend revisions that retain much of the traditional tribal structure and recognize five subfamilies instead of the traditional two subfamilies. The revised monophyletic taxonomy of myctophids includes the elevation of three former lampanyctine tribes to subfamilies. A restricted Lampanyctinae was recovered sister to Notolychninae. These two clades together were recovered as the sister group to the Gymnoscopelinae. Combined, these three subfamilies were recovered as the sister group to a clade composed of a monophyletic Diaphinae sister to the traditional Myctophinae. Our results corroborate recent multilocus molecular studies that infer a polyphyletic Myctophum in Myctophinae, and a para- or polyphyletic Lampanyctus and Nannobrachium within Lampanyctinae. We resurrect Dasyscopelus and Ctenoscopelus for the independent clades traditionally classified as species of Myctophum, and we place Nannobrachium into the synonymy of Lampanyctus.
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Patterns of Phenotypic Variation in the Mouth Size of Lanternfishes (Teleostei: Myctophiformes)
Article
  • Nov 2016
  • COPEIA
Lanternfishes (Myctophiformes, ~260 species) are among the most abundant and species-rich groups of fishes endemic to the deep sea, and they play a major role in the oceanic ecosystem by transferring energy from shallower to deeper oceanic levels. Little is currently known regarding how lanternfishes have achieved such high species richness in the deep sea, and the majority of previous studies that have investigated diversification in this group have focused on bioluminescence. In this study, we investigate the variation in mouth size of lanternfishes in an effort to better understand potential mechanisms of speciation in this group, as previous studies have indicated that there is considerable variation in the size and biodiversity of prey items of lanternfishes. Geometric morphometrics were performed on 955 lanternfish specimens, and an ancestral character-state reconstruction was used to examine variation and evolution of mouth size in this group. We identify that mouth size in lanternfishes is highly variable, with general trends towards larger mouths in the subfamily Lampanyctinae (Myctophidae) and shorter mouths in the subfamily Myctophinae (Myctophidae). Within each subfamily there are discrete patterns of jaw-size differentiation among genera. Of particular note, the genus Diaphus, the most species-rich genus of lanternfishes (~30% of lanternfish diversity), was found to occupy a large range of morphospace, with broad plasticity in mouth size among the examined species. Ancestral character-state reconstructions indicate that a neoscopelid-like jaw was the likely ancestral state for Myctophiformes; whereas, a longer jaw, similar to that of the majority of species in the subfamily Lampanyctinae, was most likely the ancestral state for the family Myctophidae.
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