Evaluating food metrics of lanternfishes in waters of the southeastern Pacific Ocean

doi:10.21203/rs.3.rs-1999213/v1

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Evaluating food metrics of lanternfishes in waters of the southeastern Pacific Ocean

https://doi.org/10.21203/rs.3.rs-1999213/v1

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published 09 Jan, 2023

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Using carbon and nitrogen stable isotope values, we analyzed the trophic position (TP) and the isotopic niche width of lanternfishes from three different fishing grounds in the Southern Pacific Ocean. Fishes from Perú had slightly higher δ13C values compared with fish from Chilean fisheries grounds. In contrast, δ15N values increased with latitude (North to South). Myctophids TP differed between the three fishing grounds (highest in Central Chile, lowest in Peru). Peruvian fishes had a smaller isotopic niche than the lanternfishes of the Chilean fishing grounds.

Myctophidae

Stable Isotopes

Trophic position

Isotopic niche

Deep-water habitats are vast ecosystems, with an estimated biomass of approximately 10 billion metric tonnes (Goetsch et al. 2018). One of the biological components contributing to this high biomass is mesopelagic fish, which inhabit depths between 200 and 1000 meters (Moteki et al. 2017; Christiansen et al. 2018; Belcher et al. 2019). The family Myctophidae is by far the most significant fraction of the mesopelagic fish component (Espinoza et al. 2017). For example, in the Southern Pacific Ocean (SPO), myctophids (comprising 35 species) are estimated to have a biomass of up to 200 million tonnes (Lourenco et al. 2017; Saunders et al. 2018). As a result, the SPO is considered the area with the highest abundance of myctophid fish in the world. Myctophids play a crucial role in these ecosystems since they are prey for marine mammals, birds, invertebrates, and other fish (Goetsch et al. 2018; Stewart et al. 2018).

Human demands for protein from the marine environment have continued to intensify. Consequently, many fish stocks are at risk of collapse (FAO 2018), and there is a pressing need to find unexploited fish stocks that can help supply this demand. SPO myctophids have been identified as a potential resource for future exploitation (Valinassab et al. 2007), but relatively little is known about their basic biology, including their trophic ecology. Here, we use stable isotopes of carbon and nitrogen to characterize key features of the trophic ecology of South Pacific myctophids prior to their commercial exploitation, including the isotopic niche and trophic position (TP). The transfer of energy and nutrients from the bottom to top links makes TP a critical concept used to describe the functional role of consumers in a food web (Quezada-Romegialli et al. 2018).

TP has historically been estimated via stomach contents through the mass and the number of prey, but those results can be over-or under-estimated due to consumer digestive biases (Hetherington et al. 2017). In recent decades, stable isotope analyses (SIA) of nitrogen (δ¹⁵N) and carbon (δ¹³C) have been used as a complementary approach that can reduce biases associated with stomach contents analysis. Values of predator stable isotope composition revealed by SIA reflect prey assimilation (Goetsch et al. 2018). A consumer’s carbon stable ratios typically reflect the primary production mode fueling the taxa comprising its diet. Meanwhile, δ¹⁵N values can be considered an indicator of TP occupied by prey and their consumers (Fry 2013). For instance, in tropical Atlantic waters, Olson and Watters (2003) examined TP in Myctophum nitidulum and Symbolophorus reversus using stomach contents, estimating a mean TP of 3.2. In contrast, stable isotopes estimated the same species to have a TP of 2.6 and 2.7, respectively (Hetherington et al. 2017).

Stable isotope values can also be used to estimate the isotopic niche - a compelling alternative to Elton’s (1927) traditional definition of the trophic niche (Cherel et al. 2010). Layman et al. (2007a) developed quantitative methods using stable isotopes to measure trophic community structure. This isotopic approach is established on how individuals’ chemical composition is directly influenced by what they consume. Therefore, predators with high δ¹⁵N values will have a higher TP, hence a wide isotopic niche size (Herzka 2005). Thus, the variability in TP values displayed by a species could determine the size of the isotopic niche and provide a broader view of the species life history characteristics. We calculated TP and the isotope niche of the most abundant lanternfishes on three different fishing grounds in the southeastern Ocean Pacific to compare their ecological function.

Samples collection

We analyzed a total of 123 individuals captured during a fisheries-independent research survey in 2015. The study area was divided into three fishing zones (Fig. 1): Peru (n = 50), Central-Chile (n = 39), and South-Chile (n = 34). A midwater trawl captured all fish from a depth range between 200 and 300 meters. After capture, they were labeled and frozen at -20°C until further analysis in the laboratory. We also collected water and zooplankton samples. For this purpose, 20 liters of water and a random set of zooplankton (plankton net WP2, ring diameter of 57 cm; mesh with 1.5 µm and length 2.6 m) were taken. The water was stored under total darkness, while the zooplankton was filtered, separated, dehydrated, and then stored under vacuum.

Lab Work

Myctophids were thawed and identified (Table 1). Approximately one gram of muscle tissue was taken from each individual. Seawater samples were filtered in the laboratory and divided into two fiberglass filters (FGP Whatman™ 1.5µm, 4.7 cm). The filter for δ¹³C was placed in a desiccator with 20 ml of 37% HCL to remove inorganic carbon; meanwhile, the filter for δ¹⁵N was put in aluminum foil at -80°C (Feuchtmayr and Grey 2003; Lorrain et al. 2003). The particulate organic matter (POM) and zooplankton left in the filters were removed and placed in individual plates. Then, all samples were dried (55°C for 48 hours) and pulverized. Subsamples of 400–500 µg were deposited in tin capsules and then analyzed in a mass spectrometer in continuous flow mode (CF) "Nu-Instruments," coupled with an elemental analyzer (EA) of Eurovector, EA-3024. Isotope radios were reported in δ notation, using standard Pee Dee Belemnite for δ¹³C and Atmospheric Nitrogen for δ¹⁵N. Therefore, δ¹³C or δ¹⁵N= [(R sample/R standard) − 1], where R is ¹³C/¹⁴C or ¹⁵N/¹⁴N, respectively. This analysis had an accuracy ± 0.1‰ for δ¹⁵N and δ¹³C.

Table 1

Summary results from δ¹³C and δ¹⁵N values of lanternfishes in the different fishing zones.
Species	Fishing ground	δ¹³C	δ¹⁵N	Range C:N	n
Ceratoscopelus warmingii	Perú	-18.2	10.7	3.54–3.69	20
Hygphum proximum		-18.4	11.6		20
Myctophum aurolaternatum		-18.3	11.3		10
Ceratoscopelus warmingii	Central-Chile	-17.3	17.7	3.64–6.03	10
Diogenichthys atlanticus		-18.8	15.0		5
Gymnoscopelus sp.		-18.8	15.7		5
Hintonia candens		-17.4	15.8		15
Hygphum proximum		-18.3	13.9		4
Diaphus hudsoni	South-Chile	-18.7	17.4	5.41–6.31	1
Electrona subaspera		-19.8	10.1		5
Hygphum proximum		-18.5	15.1		1
Lampadena luminosa		-18.1	13.8		3
Lampanyctodes sp.		-18.6	14.5		1
Lampanyctodes hectoris		-18.3	14.6		5
Myctophum sp.		-19.7	13.7		2
Protomyctophum tenisoni		-21.7	6.6		10
Symbolophorus boops		-18.4	13.1		5
Taaningichtys bathyphilus		-18.1	18.1		1
Baselines
Copepods	Perú	-20.5	7.9	4.74	11*
Copepods	Central-Chile	-21.5	11.0	3.21	22*
Copepods	South-Chile	-20.7	12.5	3.75	15*
POM	Perú	-22.8	3.9	-	21*
POM	Central-Chile	-24.8	2.9	-	10*
POM	South-Chile	-24.5	4.3	-	25*
* Numbers of filters					Total 227

Data analysis

We calculated trophic position (TP) using two contrasting taxa as baselines based on the bulk SIA values. First, we assumed POM TP (λ) as one and copepods TP as λ = 2. Then, using the “tRophicPosition” package with Bayesian inference by the One baseline model (Quezada-Romegialli et al. 2018), we calculated myctophid TP for each of the three zones using a trophic discrimination factor (TDF) of ± SD (Δ¹⁵N) of 3.4 ± 1‰ (Post 2002). Therefore, TP was calculated following this equation:

$$TP=[ {({\delta }}^{15}{\text{N}}_{M} - {{\delta }}^{15}{\text{N}}_{b})/ {{\Delta }}^{15}\text{N}\left)\right] + {\lambda }$$

where δ¹⁵N_M and δ¹⁵N_b refer to the nitrogen values of the myctophids (M) and baseline (b), respectively, the standard ellipse area (SEA), followed by a convex-hull analysis was estimated to infer the isotopic niche’s amplitude (Layman et al. 2007b). The “SIBER” package with Bayesian inference was used for this analysis (Jackson et al. 2011). A PERMANOVA: n_permutations =9.999 test was used, based on a Euclidean similarity matrix to compare the values of δ¹⁵N and δ¹³C. A general linear model (GLM) was used to compare the values of δ¹⁵N and SEA of myctophids in the different fishing zones, and a one-way ANOVA was applied to compare the mean values of POM and copepods.

Myctophids showed differences in estimated TP between the three fishing grounds. POM δ¹³C values from the Peruvian fishing ground were ¹³C-enriched (ANOVA; F_(1,24) = 8.31, P = 0.029) compared to samples from central-Chile and south-Chile (Table 1). In turn, δ¹⁵N POM values were higher in south Chile (ANOVA; F_(1,25) = 10.28, P = 0.012). Copepod δ¹³C and δ¹⁵N did not vary among fishing grounds (ANOVA; F_(1,23) = 13.58, P = 0.116). However, stable isotope composition varied with the fishing ground (PERMANOVA; F = 99.63, P = 0.003). Perú is intermediated fish between the two Chilean ranges, but not significant, δ¹³C values (Fig. 2), meanwhile the δ¹⁵N values increased with latitude (Table 2). SEA not increased towards high latitudes. Indeed, SEA of central-Chile was larger than Peru and south-Chile; Peru vs. Central-Chile (GLM; t_− 2.270; P = 0.019) than central-Chile vs. South-Chile (GLM; t_2.674; P = 0.021(Fig. 3a).

Table 2

Results of Bayesian analysis of trophic position analysis from two different baselines, POM (TP_POM) and Copepods (TP_Copepods)and size of the isotopic niche as standard ellipse area (SEA). SD; standard deviation and CI; credible intervals.
Fishing ground	TP_POM		TP_Copepods		SEA
	Mean (± SD)	95% CIs	Mean (± SD)	95% CIs	Mean (± SD)	95% CIs
Peru	3.03 (0.35)	2.25, 3.73	2.87 (0.36)	2.09, 3.57	2.22 (0.31)	2.17, 2.27
Central-Chile	4.93 (0.93)	2.24, 6.25	3.57 (0.93)	2.11, 4.98	12.26 (2.40)	12.21, 12.31
South-Chile	3.85 (0.90)	2.48, 5.17	2.44 (0.90)	2.93, 3.75	7.07 (0.96)	7.02, 7.12

The average TP estimates using POM as the baseline (TP_POM) varied in higher ranges than those TP estimates based on copepods (TP_copepods) (Table 2). The posterior Bayesian TP calculated for Pacific myctophids for each fishing ground were similarly dependent on the baseline (Fig. 3b). This variation could be by many factors, such as feeding rates, tissues turnover rates, and/or trophic enrichment factors. Our finding to TP (~ 2.5) of lanternfishes in the SPO was similar to those obtained in other works for analogous species (Cherel et al. 2010; Bernal et al. 2015; Hetherington et al. 2017). Although the Peruvian and Chilean mesopelagic zones are considered similar oceanographically (Sutton et al. 2017), lanternfishes from the different fishing grounds showed differences in their stable isotope values. These differences likely reflect regional differences in upwelling. For example, the region of Peru sampled here has a seasonal pulse of upwelling. In contrast, the Chilean areas are subject to more permanent upwelling and, therefore, a continuous pattern of elevated primary production, explaining the isotopically enriched POM (Gutiérrez et al. 2016). Indeed, Pizarro et al. (2019) reported ¹⁵N-enriched POM values in Northern Chile and associated this with upwelling.

The Southern Pacific Ocean’s lanternfishes could play an active and key role in carbon flow in the trophic web as these fishes represent prey for predators associated with different marine habitats, including surface and deep waters. In fact, Hudson et al. (2014) proposed the proportion of carbon flux carried out by the lanternfish at greater depths confirms the importance of myctophids in the biological pump of deep sea zones of the Atlantic Ocean. Olivar et al. (2019) describe secondary consumers’ role in the deep-sea ecosystem, in which some species have a vertical migration in the water column. Castro et al. (2010) found the same behavior in some lanternfishes of the SPO. This behavior results in myctophid fishes transferring energy from the upper layers of water towards the depths. Conversely, when lanternfishes migrate to the surface, they are prey for pelagic predators, including penguins, sharks, and marine mammals. However, when they migrate into deeper waters, they are prey for mesopelagic predators such as hake and squid. Therefore, our results point out that the lanternfishes from SPO likely play a primary role in the energy flow from deep waters to the surface. Nevertheless, future work is needed on lanternfishes. While myctophids are typically considered as a single homogenous guild, there are doubtless ways in which the species have differentiated. Given that our results show spatial differences in the ecological function of the guild, future studies in the SPO should compare the trophic ecology of individual species across different areas.

Acknowledgments

The authors are grateful for the valuable work done by the scientific observers of IFOP and IMARPE on the research vessels.

Consent to publish

This work did not have any person as a study subject.

Consent to participate

This work did not have any person as a study subject.

Funding

Author SK has received support from IFOP-SUBPESCA:2015: “Interacciones tróficas entre la jibia (Dosidicus gigas) y la merluza común (Merluccius gayi) en aguas frente a chile central” and IFOP-SUBPESCA: 2015/1049-24: “Composición e importancia de los principales ítems alimentarios de merluza del sur, merluza de cola y merluza de tres aletas entre la X y XII Regiones de Chile, año 2015”. CH was supported by Núcleo Milenio INVASAL (NCN16_034) funded by ANID Millennium Science Initiative Programme.

Author Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Sebastian A. Klarian, Ivonne Quintanilla, Fernanda Vargas, Pepe Espinoza, Mauricio Zuñiga, Patricio Galvez, Rene Vargas, Alvaro Saavedra, Stephanny Curaz-Leiva. The first draft of the manuscript was written by Sebastian A. Klarian, Carolina Carcamo, Eric Schultz, Pepe Espinoza, Chris Harrod, Francisco Fernandoy, Ana Guzman, Carlos Canales-Cerro and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Ethics approval

The authors from the competent authorities have obtained all necessary permissions for sampling and observational field studies. The research cruises counted all the legal authorizations for fishing research that Perú and Chile’s laws maintain in their territory.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Belcher A, Saunders RA, Tarling GA (2019) Respiration rates and active carbon flux of mesopelagic fishes (Family Myctophidae) in the Scotia Sea, Southern Ocean. Mar Ecol Prog Ser 610:149–162. doi: 10.3354/meps12861
Bernal A, Olivar MP, Maynou F, Luz Fernandez de Puelles M (2015) Diet and feeding strategies of mesopelagic fishes in the western Mediterranean. Prog Oceanogr 135:1–17. doi: 10.1016/j.pocean.2015.03.005
de Castro MS, Richards WJ, Bonecker ACT (2010) Occurrence and distribution of larval lanternfish (Myctophidae) from the southwest Atlantic Ocean. Zoologia 27:541–553. doi: 10.1590/S1984-46702010000400006
Cherel Y, Fontaine C, Richard P, Labatc J-P (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr 55:324–332. doi: 10.4319/lo.2010.55.1.0324
Christiansen H, Dettai A, Heindler FM, Collins MA, Duhamel G, Hautecoeur M, Steinke D, Volckaert FAM, Van de Putte AP (2018) Diversity of Mesopelagic Fishes in the Southern Ocean - A Phylogeographic Perspective Using DNA Barcoding. Front Ecol Evol 6:120. doi: 10.3389/fevo.2018.00120
Elton CS (1927) Animal ecology. Sidgwick & Jackson, London
Espinoza P, Lorrain A, Ménard F, Cherel Y, Tremblay-Boyer L, Argüelles J, Tafur R, Bertrand S, Tremblay Y, Ayón P, Munaron J-M, Richard P, Bertrand A (2017) Trophic structure in the northern Humboldt Current system: new perspectives from stable isotope analysis. Mar Biol 164:86. doi: 10.1007/s00227-017-3119-8
FAO (2018) The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. Food and Agriculture Organization of the United Nations
Feuchtmayr H, Grey J (2003) Effect of preparation and preservation procedures on carbon and nitrogen stable isotope determinations from zooplankton. Rapid Commun Mass Spectrom 17:2605–2610. doi: 10.1002/rcm.1227
Fry B (2013) Using stable CNS isotopes to evaluate estuarine fisheries condition and health. Isot Environ Health Stud 49:295–304. doi: 10.1080/10256016.2013.783830
Goetsch C, Conners MG, Budge SM, Mitani Y, Walker WA, Bromaghin JF, Simmons SE, Reichmuth C, Costa DP (2018) Energy-Rich Mesopelagic Fishes Revealed as a Critical Prey Resource for a Deep-Diving Predator Using Quantitative Fatty Acid Signature Analysis. Front Mar Sci 5:430. doi: 10.3389/fmars.2018.00430
Gutiérrez D, Akester M, Naranjo L (2016) Productivity and Sustainable Management of the Humboldt Current Large Marine Ecosystem under climate change. Environ Dev 17:126–144. doi: 10.1016/j.envdev.2015.11.004
Herzka SZ (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuar Coast Shelf Sci 64:58–69. doi: 10.1016/j.ecss.2005.02.006
Hetherington ED, Olson RJ, Drazen JC, Lennert-Cody CE, Ballance LT, Kaufmann RS, Popp BN (2017) Spatial food-web structure in the eastern tropical Pacific Ocean based on compound-specific nitrogen isotope analysis of amino acids. Limnol Oceanogr 62:541–560. doi: 10.1002/lno.10443
Hudson JM, Steinberg DK, Sutton TT, Graves JE, Latour RJ (2014) Myctophid feeding ecology and carbon transport along the northern Mid-Atlantic Ridge. Deep-Sea Res Part I-Oceanographic Res Papers 93:104–116. doi: 10.1016/j.dsr.2014.07.002
Jackson AL, Inger R, Parnell AC (2011) Comparing isotopic niche widths among and within communities. SIBER–Stable Isotope Bayesian Ellipses in R
Layman CA, Arrington DA, Montaña CG, Post DM (2007a) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. doi: 10.1890/0012-9658(2007)88[42:csirpf]2.0.co;2
Layman CA, Quattrochi JP, Peyer CM, Allgeier JE (2007b) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett 10:937–944. doi: 10.1111/j.1461-0248.2007.01087.x
Lorrain A, Savoye N, Chauvaud L, Paulet Y-M, Naulet N (2003) Decarbonation and preservation method for the analysis of organic C and N contents and stable isotope ratios of low-carbonated suspended particulate material. Anal Chim Acta 491:125–133. doi: 10.1016/S0003-2670(03)00815-8
Lourenco S, Saunders RA, Collins M, Shreeve R, Assis CA, Belchier M, Watkins JL, Xavier JC (2017) Life cycle, distribution and trophodynamics of the lanternfish Krefftichthys anderssoni (Lonnberg, 1905) in the Scotia Sea. Polar Biol 40:1229–1245. doi: 10.1007/s00300-016-2046-3
Moteki M, Tsujimura E, Hulley P-A (2017) Developmental intervals during the larval and juvenile stages of the Antarctic myctophid fish Electrona antarctica in relation to changes in feeding and swimming functions. Polar Sci 12:88–98. doi: 10.1016/j.polar.2017.02.006
Olivar MP, Bode A, López-Pérez C, Hulley PA, Hernández-León S (2019) Trophic position of lanternfishes (Pisces: Myctophidae) of the tropical and equatorial Atlantic estimated using stable isotopes. ICES J Mar Sci 76:649–661. doi: 10.1093/icesjms/fsx243
Olson JR, Watters MG (2003) A model of the pelagic ecosystem in the eastern tropical Pacific Ocean. Bull IATTC/Bol CIAT 22:133–217
Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C (2018) tRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592–1599. doi: 10.1111/2041-210X.13009
Saunders RA, Collins MA, Shreeve R, Ward P, Stowasser G, Hill SL, Tarling GA (2018) Seasonal variation in the predatory impact of myctophids on zooplankton in the Scotia Sea (Southern Ocean). Prog Oceanogr 168:123–144. doi: 10.1016/j.pocean.2018.09.017
Stewart JD, Barroso A, Butler RH, Munns RJ (2018) Caught at the surface: myctophids make easy prey for dolphins and devil rays. Ecology 99:1894–1896. doi: 10.1002/ecy.2348
Sutton TT, Clark MR, Dunn DC, Halpin PN, Rogers AD, Guinotte J, Bograd SJ, Angel MV, Perez JAA, Wishner K, Haedrich RL, Lindsay DJ, Drazen JC, Vereshchaka A, Piatkowski U, Morato T, Błachowiak-Samołyk K, Robison BH, Gjerde KM, Pierrot-Bults A, Bernal P, Reygondeau G, Heino M (2017) A global biogeographic classification of the mesopelagic zone. Deep Sea Res Part I 126:85–102. doi: 10.1016/j.dsr.2017.05.006
Valinassab T, Pierce GJ, Johannesson K (2007) Lantern fish (Benthosema pterotum) resources as a target for commercial exploitation in the Oman Sea. J Appl Ichthyol 23:573–577. doi: 10.1111/j.1439-0426.2007.01034.x

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Journal Publication

published 09 Jan, 2023

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Editorial decision: Acceptable after minor revision
14 Nov, 2022
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You are reading this latest preprint version

Evaluating food metrics of lanternfishes in waters of the southeastern Pacific Ocean

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Journal Publication

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Abstract

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Introduction

Material And Methods

Samples collection

Lab Work

Data analysis

Results And Discussion

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References

Status:

Journal Publication

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