SciELO - Scientific Electronic Library Online

vol.51 issue2Incidental capture of the short-beaked common dolphin (Delphinus delphis) in the industrial purse seine fishery in northern ChilePachygrapsus transversus in Easter Island, What species are we talking about? (Decapoda, Brachyura, Grapsoidea) author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand




Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google


Revista de biología marina y oceanografía

On-line version ISSN 0718-1957

Rev. biol. mar. oceanogr. vol.51 no.2 Valparaíso Aug. 2016 



First measurements of euphausiid growth rates in the northern Humboldt Current (23ºS)

Primeras mediciones de tasas de crecimiento de eufáusidos en el norte de la Corriente de Humboldt (23ºS)


Ramiro Riquelme-Bugueño1,2*, Jaime Gómez-Gutiérrez3, Rubén Escribano2,4, Paula Ruz2,5, Pamela Hidalgo2,4 and Wolfgang Schneider2,4

1Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, CP 160-C, Concepción, Chile
2Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile. *
3Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Departamento de Plancton y Ecología Marina, La Paz, Baja California Sur, CP 23096, México
4Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, CP 160-C, Concepción, Chile
5Programa de Doctorado en Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, CP 160-C, Concepción, Chile


One hundred and five juveniles and adults of Euphausia mucronata were incubated in order to estimate their daily growth rates (DGR) using the standard instantaneous growth rate method. From 77 krill that survived after 2 days of incubation under laboratory conditions, 70 individuals molted (35.1% males, 64.9% females). E. mucronata mean intermolt period was 5.2 days (range = 4-9 d) with mean DGR of 0.01 mm d-1 for males and -0.04 mm d-1 for females. Overall mean DGR was -0.02 mm d-1. DGRs were positive (31%), zero (12%) and negative (57%). DGR<0 evidenced body shrinking process suggesting that environmental conditions in austral autumn 2010 were unfavorable for the krill population. However, because females had DGR<0 values more frequently than males it is probable that females also used part of their energy on gonad development rather than body growth.

Key words: Euphausia mucronata, intermolt period, Bahía Mejillones, Southeastern Pacific, Chile


Euphausiids (or krill) are small pelagic crustaceans similar in shape to shrimps. Several species form immense aggregations being a key component in the marine pelagic food web by channeling organic matter from lower to higher trophic levels (Everson 2000, González et al. 2009, Antezana 2010). Their ecology and biology have been broadly studied in the world ocean (Brinton et al. 2000, Everson 2000), but most knowledge on ecology and biology come mainly from studies of the Antarctic krill (Euphausia superba) or krill species in the northern hemisphere. In the past it was though that euphausiid always increase size (somatic growth) between successive ecdysis events; however, since the 1980's decade it was demonstrated that euphausiids do not growth or even shrink between two successive molting events. Ikeda & Dixon (1982) were the first scientists to report shrinking (they called negative growth) in the subtropical euphausiid Nyctiphanes australis based on body length and physiological rate measurements using incubated specimens under laboratory conditions. This phenomenon has usually been interpreted as a response of krill to suboptimal environmental conditions (temperature, food) and/or as an alternative source of energy for gonad development (reproduction) and growth during periods of scarce food (as an overwintering strategy) (Ikeda & Dixon 1982, Quetin & Ross 1991). However, experimental evidence suggests that shrinking in krill occur throughout the year round in polar (Nicol 2000, Tarling et al. 2006), temperate (Pinchuck & Hopcroft 2007, Feinberg et al. 2007, Shaw et al. 2010, Pond et al. 2012, Riquelme-Bugueño et al. 2016), and subtropical krill species (Gómez-Gutiérrez et al. 2012). These studies, among others, provide evidence that: 1) growth in krill is not necessarily limited by food but in occasions caused by anomalous changes in temperatures (Marinovic & Mangel 1999), 2) growth is highly variable at intraspecific and interspecific levels and body growth rates in females is negative correlated with brood size and interbrood periods (Feinberg et al. 2007), and 3) positive, zero and negative growth should occur in any krill species because this physiological process have been observed in species from distinct biogeographic affinities (Atkinson et al. 2006, Tarling et al. 2006, Shaw et al. 2010, Gómez-Gutiérrez et al. 2012, Pond et al. 2012).

Euphausia mucronata is the most abundant, widely distributed and ecologically relevant krill species in the Humboldt Current System (HCS) (Antezana 2010, Riquelme-Bugueño et al. 2012, 2013). Riquelme-Bugueño et al. (2013) estimated the E. mucronata intermolt period from specimens collected during austral spring 2007 and summer 2008 using the 1/MR standard method (Tarling et al. 2006). They estimated secondary production (body and egg production rates) using the cohort analysis from a monthly time series at a station off Dichato (2002-2007). However, these methods are, by definition, mean population estimations of growth rates and intermoult period rather than individual measurements representative of euphausiid physiological status under certain local environmental conditions. Thus, the magnitude and variability of individual E. mucronata growth rates has not been yet estimated. The aim of the present study was to do the first report in the HCS of the intermolt period and instantaneous growth rate of E. mucronata measured under laboratory conditions.



Euphausia mucronata specimens were captured at night onboard the boat Marlin in Bahía Mejillones, Antofagasta, Chile (23ºS, Fig. 1) during May 10-30, 2010. Krill sampling was made using a conical net (1 m diameter mouth and 333 µm mesh net) with a non-filtering cod-end (31.5 L). The net was deployed at a depth of 20-50 m and trawled to the surface during 10 to 20 min. Once animals were onboard, they were gently placed in a cooler and transported to a land-based laboratory equipped with cold rooms. The incubation was conducted either onboard or at land <2 h after sampling. In total 105 E. mucronata individuals were incubated from 3 nocturnal samplings. The euphausiids were incubated individually in ~800 ml transparent plastic jars containing filtered seawater (100 µm). The jars were kept in darkness in a cold room at 11-12°C, which was the sea surface temperature recorded in situ with a portable temperature sensor (SevenGo, Mettler Toledo). Incubations lasted 48 h to avoid laboratory artifacts with food deprivation (Shaw et al. 2006, 2010; Gómez-Gutiérrez et al. 2012) and each incubated euphausiid was checked for molting at 12 h intervals. Males were identified by examining the presence of spermatophores or the petasma located in the first pair of abdominal appendages and females were identified by observing their thelycum or presence of spermatophores attached on their thelycum (Brinton et al. 2000). Seawater was changed every 24 h. When molts were present these were separated together with animals and later measured the telson and uropod lengths. The instantaneous growth rate (IGR) technique was used to estimate growth rates (Ross et al. 2000). This technique consists of measuring the difference between the length of the telson (and/or uropod) of the animal and of the molt during the laboratory incubation (Shaw et al. 2006, 2010, Fig. 2). The telson of the animal and the molt are generally used because the telson is usually the best preserved structure in comparison with the rest of the structures of the discarded molt (also known as exuvia). The telson lengths of the animal and the molt were measured immediately after molt was detected in the incubation bottles. When it was not possible to do measurements when molting occurred, the animal and molt were preserved in a 10% formalin solution for later measurements. Measured molt length (ML) was transformed to total length (TL) following Melo & Antezana (1980) equation. The standard IGR method (Tarling et al. 2006) was used to estimate the E. mucronata growth increment (GI, in %) as follows:

where Ta and Tm are the telson length of the animal and molt, respectively. Ta and Tm were measured with a lateral view from the posterior part of the sixth abdominal segment to the tip of telson. DGR (mm d-1) was then calculated based on Tarling et al. (2006) method as:

where Lpre is the estimated total length (TL) before molt of the animal (mm), GI is the growth increment, and IMP is the intermolt period. Lpre was derived from a TL-telson equation from Melo & Antezana (1980). IMP was calculated using the 1/MR method (Tarling et al. 2006):

where N is the total number of krill that were alive at the end of the experiment plus krill that molted during the incubation period, Nm is the number of krill specimens that molted, and t is the duration of the incubation period (2 days). All length measurements were done using a stereomicroscope equipped with a calibrated micrometer.


Figure 1. Study area in Bahía de Mejillones, located northern region of the Humboldt
Current System (Antofagasta, Chile), showing the site (black cross) where
specimens of Euphausia mucronata were sampled in May 2010
Figura 1. Área de estudio en Bahía de Mejillones, localizado en la región norte de la Corriente
de Humboldt (Antofagasta, Chile), mostrando el sitio (cruz negra) donde especímenes de
Euphausia mucronata
fueron muestreados en mayo 2010


Figure 2. Euphausia mucronata. a) incubated specimen, b) specimen showing its molt after
the molting event, c) lateral view showing how the telson length of each specimen
was measured, d) dorsal view of measurements of the telson length
Figura 2. Euphausia mucronata. a) espécimen incubado, b) espécimen mostrando su muda después
del evento de ecdisis, c) vista lateral mostrando cómo se realizaron las mediciones de la longitud
del telson en cada individuo, d) vista dorsal de las mediciones de la longitud del telson


The instantaneous growth rate (IGR) method assumes that 1) field sampling (with the net of big cod-end and drifting tow) and field-to-laboratory transport conditions do not cause significant stress, 2) growth rates measured under laboratory reflect what animals feed on a natural conditions (phytoplankton and microzooplankton) before zooplankton sampling, and 3) that incubated individuals were not under starvation for a significant period of time. Thus, we assume that measured instantaneous growth rates are representative of the growth rates that occur at nature (Tarling et al. 2006).

We tested statistical differences in DGR between male and female using an ANOVA test and descriptive summary is presented by mean of a box-and-whisker plots. Analyses and plots were done using STATISTICA 8 software.



From 105 E. mucronata incubated specimens, 77 of them survived (73.3%) after 2 days of incubation. From these survivors, 70 individuals molted during incubations including 25 males (35.1%) and 45 females (64.9%). Mean total length was similar for males and females (~15 mm TL), although the standard deviation (SD) and range were wider for males than for females (Fig. 3a). Mean IMP was 5.2 days (± 1.5 SD), ranging from 4 to 9 days, which is within the mean of 4 days (range: 4-6 days) estimated by Antezana & Melo (2008). Our IMP estimations were similar to those reported for the temperate species E. pacifica estimated during upwelling (mean = 8 days) and downwelling (mean = 11 days) seasons from a 7-years' time series carried out off the Oregon coast (Shaw et al. 2010). E. mucronata mean GI was 0.73% (± 5.12 SD) for males and -1.62% (± 3.96 SD) for females. Mean DGR was 0.01 mm d-1 (± 0.13 SD) in males and -0.04 mm d-1 (± 0.10 SD) in females (Figs. 3b, c). Shaw et al. (2010) reported mean E. pacifica DGRs of 0.02 mm d-1 for the upwelling and 0.01 mm d-1 for the downwelling seasons. Pooling all the males and females data from our experiment, mean GI was -0.83% (± 4.46 SD) and mean DGR was -0.02 mm d-1 (± 0.11 SD). All our measurements were comparable to those reported in other studies on krill growth rates (Shaw et al. 2010, Gómez-Gutiérrez et al. 2012). No significant differences of TL, GI and DGR were found between E. mucronata males and females (ANOVA, P > 0.05). A high degree of individual variability was observed in our measurements corresponding 31% to individuals growing (DGR>0), a 12% with DGR= 0 and, a 57% with DGR<0 (i.e., shrinking) evidencing how the population has individuals with different capabilities to obtain energy from its habitat and how respond to local environmental conditions. Hosie & Ritz (1989) also observed shrinkage in Nyctiphanes australis, with >70% of incubated individuals experimenting decreased body size, apparently because of poor food quality or lack of feeding in nature. Negative DGR has been attributed to krill populations under unfavorable environmental conditions, such as unusually high temperature (Marinovic & Mangel 1999) and limited food availability (Virtue et al. 2010, Gómez-Gutiérrez et al. 2012), or as an overwinter strategy (Ikeda & Dixon 1982, Daly 2004). However, experimental evidence suggests that negative growth is commonly observed in krill during their life cycle and occurring in any season of the year in polar (Tarling et al. 2006), temperate (Marinovic & Mangel 1999, Shaw et al. 2010), and subtropical ecosystems (Gómez-Gutiérrez et al. 2012). Most recent field work (2011_2014) off Dichato coast provided a comparative frame of reference of E. mucronata growth rates (Riquelme-Bugueño et al. 2016) with our measurements observed in the northern HCS. In our study, DGR did not show a significant relationship with TL (data not shown). Body shrinkage in females may reflect the allocation of energy to gonad development (reproduction) rather than somatic growth (Atkinson et al. 2006, Feinberg et al. 2007). However, during our sampling effort we did not observe gravid females (females with blue or purple gonad) or spawned.


Figure 3. Box-and-whisker plots indicating the descriptive statistical (mean,
standard deviation and range) of Euphausia mucronata: a) total
length (TL), b) growth increment (GI) and c) daily growth rate (DGR),
measured in females and males during incubations under laboratory
conditions carried out in May 2010
Figura 3. Diagrama de caja indicando la estadística descriptiva (promedio, desviación
estándar y rango) de: a) longitud total (TL), b) incremento en crecimiento (GI) y
c) tasa de crecimiento diaria (DGR) de machos y hembras de Euphausia
durante incubaciones bajo condiciones de
laboratorio realizadas en mayo 2010


Direct measurements of vital rates of individuals incubated under laboratory conditions, such as the body growth rate and intermolt periods, have improved estimations of total secondary production because provide credible data input to models about how animals respond to local conditions (Tarling et al. 2006, Gómez-Gutiérrez et al. 2012, Riquelme-Bugueño et al. 2013). Ongoing monitoring efforts will help to better understand the ecological function of E. mucronata in the secondary productivity and biomass contribution in this coastal upwelling ecosystem and its co-variation with spatio-temporal environmental conditions. In the future, studies using the hepato-somatic index (relative size of the digestive gland in the relation of cephalothorax size) and lipid content analyses will provide also useful information to know the recent nutritional history in this krill species. Because respiration accounted for the major portion of the assimilation of carbon of E. pacifica (62-87%) and molting, growth, and reproduction accounted for the remainder (Lasker 1966) as was done for this species in Japan (Iguchi & Ikeda 1995), future studies should also estimate respiration rates of E. mucronata. The results of the present study confirm how krill populations display considerably high individual variability in observed krill growth rates independently of the species, sex, regions and seasons. This challenges the integrative understanding about how krill respond to local conditions and how they can transform their energy into biomass available to their natural predators, several of them of commercial interest for human consumption.



This study was funded by FONDECYT 1080037 grant (R.E.). R.R-B was supported by the CONICYT 21080484, 24110048 scholarships and, J.G-G was supported by CONACyT (CB-2012-178615-01), SNI, COFAA-IPN, and EDI-IPN grants. Additional support was provided by FONDECYT 3130387 (R.R-B) and USA 2012-0006 grant (P.H.). This study is a contribution of the Instituto Milenio de Oceanografía (IC120019).



Antezana T. 2010. Euphausia mucronata: A keystone herbivore and prey in the Humboldt Current System. Deep Sea Research II 57(7-8): 652-662.         [ Links ]

Antezana T & C Melo. 2008. Larval development of Humboldt Current krill, Euphausia mucronata G. O. Sars, 1883 (Malacostraca, Euphausiacea). Crustaceana 81(3): 305-328.         [ Links ]

Atkinson A, R Shreeve, A Hirst, P Rothery, G Tarling, D Pond, R Korb, E Murphy & J Watkins. 2006. Natural growth rates in Antarctic krill (Euphausia superba): II. Predictive models based on food, temperature, body length, sex, and maturity stage. Limnology and Oceanography 51: 973-987.         [ Links ]

Brinton E, M Ohman, A Townsend, M Knight & A Bridgeman. 2000. Euphausiids of the world ocean. World Biodiversity Database. Expert Center for Taxonomic Identification, Amsterdam. <>         [ Links ]

Daly K. 2004. Overwintering growth and development of larval Euphausia superba: an interannual comparison under varying environmental conditions west of the Antarctic Peninsula. Deep Sea Research II 51(17-19): 2139-2168.         [ Links ]

Everson I. 2000. Role of krill in marine food webs: The southern Ocean. In: Everson I (ed). Krill: biology, ecology and fisheries, pp 194-201, Blackwell, Oxford.         [ Links ]

Feinberg LR, CT Shaw & WT Peterson. 2007. Long-term laboratory observations of Euphausia pacifica fecundity: comparison of two geographic regions. Marine Ecology Progress Series 341: 141-152.         [ Links ]

Gómez-Gutiérrez J, S Martínez-Gómez & C Robinson. 2012. Seasonal growth, molt, and egg production of Nyctiphanes simplex (Crustacea: Euphausiacea) juveniles and adults in the Gulf of California. Marine Ecology Progress Series 455: 173-194.         [ Links ]

González H, G Daneri, J Iriarte, B Yannicelli, E Menschel, C Barria, S Pantoja & L Lizarraga. 2009. Carbon fluxes within the epipelagic zone of the Humboldt Current System off Chile: The significance of euphausiids and diatoms as key functional groups for the biological pump. Progress in
Oceanography 83(1-4): 217-227.

Hosie G & D Ritz. 1989. Body shrinkage in the subtropical euphausiid Nyctiphanes australis G.O. Sars. Journal of Plankton Research 11: 595-598.         [ Links ]

Iguchi N & T Ikeda. 1995. Growth, metabolism and growth efficiency of a euphausiid crustacean Euphausia pacifica in the southern Japan Sea, as influenced by temperature. Journal of Plankton Research 17(9): 1757-1769.         [ Links ]

Ikeda T & P Dixon. 1982. Body shrinkage as a possible over-wintering mechanism of the Antarctic krill, Euphausia superba Dana. Journal of Experimental Marine Biology and Ecology 62: 143-151.         [ Links ]

Lasker R. 1966. Feeding, growth, respiration, and carbon utilization of a euphausiid crustacean. Journal of the Fisheries Board of Canada 23(9): 1291-1317.         [ Links ]

Marinovic B & M Mangel. 1999. Krill can shrink as an ecological adaptation to temporarily unfavorable environments. Ecology Letters 2: 338-343.         [ Links ]

Melo C & T Antezana. 1980. Allometric larval relations of Euphausia mucronata Sars, 1885. Revista de Biología Marina 17(1): 135-148. Full text via         [ Links ]

Nicol S. 2000. Understanding krill growth and aging: the contribution of experimental studies. Canadian Journal of Fisheries and Aquatic Sciences 57(Suppl. 3): 168-177.         [ Links ]

Pinchuk AI & RR Hopcroft. 2007. Seasonal variations in the growth rates of euphausiids (Thysanoessa inermis, T. spinifera, and Euphausia pacifica) from the northern Gulf of Alaska. Marine Biology 151(1): 257-269.         [ Links ]

Pond D, G Tarling, K Schmidt & I Everson. 2012. Diet and growth rates of Meganyctiphanes norvegica in autumn. Marine Biology Research 8: 615-623.         [ Links ]

Quetin L & R Ross. 1991. Behavioral and physiological characteristics of Antarctic krill Euphausia superba Dana. American Zoologist 31: 49-63.         [ Links ]

Riquelme-Bugueño R, S Núñez, E Jorquera, L Valenzuela, R Escribano & S Hormazábal. 2012. The influence of upwelling variation on the spatially-structured euphausiid community off central-southern Chile in 2007-2008. Progress in Oceanography 92/95: 146-165.         [ Links ]

Riquelme-Bugueño R, R Escribano & J Gómez-Gutiérrez. 2013. Somatic and molt production in Euphausia mucronata off central-southern Chile: the influence of coastal upwelling variability. Marine Ecology Progress Series 476: 39-57.         [ Links ]

Riquelme-Bugueño R, J Silva-Aburto, R Escribano, W Peterson & W Schneider. 2016. Growth of the Humboldt Current krill in the upwelling zone off central Chile. Journal of Marine System 163: 1-11.         [ Links ]

Ross R, L Quetin, K Baker, M Vernet & R Smith. 2000. Growth limitation in young Euphausia superba under field conditions. Limnology and Oceanography 45: 31-43.         [ Links ]

Shaw CT, LR Feinberg & WT Peterson. 2006. Protocols for measuring molting rate and egg production of live euphausiids. Hatfield Marine Science Center, Newport, 15 pp. <>         [ Links ]

Shaw CT, WT Peterson & LR Feinberg. 2010. Growth of Euphausia pacifica in the upwelling zone off the Oregon coast. Deep Sea Research II 57: 584-593.         [ Links ]

Tarling G, R Shreeve, A Hirst, A Atkinson, D Pond, E Murphy & J Watkins. 2006. Natural growth rates in Antarctic krill (Euphausia superba): I. Improving methodology and predicting intermolt period. Limnology and Oceanography 51: 959-972.         [ Links ]

Virtue P, S Kawaguchi, J McIvor, S Nicol, S Wotherspoon, M Brown, R Casper, S Davenport, L Finley, J Foster, T Yoshida& T Yoshiki. 2010. Krill growth and condition in Western Indian Ocean sector of the Southern Ocean 30-80ºE in austral summer 2006. Deep-Sea Research II 57: 948-955.         [ Links ]

Received 20 August 2015 and accepted 29 March 2016
Editor: Claudia Bustos D.

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License