can upwelling signals be detected in intertidal fishes of different trophic levels?

Journal of Fish Biology (2013) 83, 1407–1415

doi:10.1111/jfb.12220, available online at wileyonlinelibrary.com

Can upwelling signals be detected in intertidal fishesof different trophic levels?

J. Pulgar*†, E. Poblete‡, M. Alvarez‡, J. P. Morales‡, B. Aranda§,M. Aldana‖ and V. M. Pulgar¶

*Departamento de Ecología & Biodiversidad, Republica 470, piso 3, Universidad AndresBello, Santiago, Chile, ‡Departamento de Ciencias Biologicas Republica 217,UniversidadAndres Bello, Santiago, Chile, §Escuela de Biología Marina, Universidad Andres Bello,Santiago, Chile, ‖Universidad Central de Chile, Escuela de Pedagogía en Biología y

Ciencias, Facultad de Ciencia de la Educacion, Santa Isabel 1278, Santiago, Chile and¶Center for Research in Obstetrics & Gynecology, Wake Forest School of Medicine and

Biomedical Research Infrastructure Center, Winston-Salem State University, Winston-Salem,NC, U.S.A.

(Received 14 March 2013, Accepted 30 July 2013)

For intertidal fishes belonging to three species, the herbivore Scartichthys viridis (Blenniidae), theomnivore Girella laevifrons (Kyphosidae) and the carnivore Graus nigra (Kyphosidae), mass andbody size relationships were higher in individuals from an upwelling zone compared with those froma non-upwelling zone. RNA:DNA were higher in the herbivores and omnivores from the upwellingzone. Higher biomass and RNA:DNA in the upwelling intertidal fishes may be a consequenceof an increased exposure to higher nutrient availability, suggesting that increased physiologicalconditioning in vertebrates from upwelling areas can be detected and measured using intertidalfishes of different trophic levels.

© 2013 The Fisheries Society of the British Isles

Key words: intertidal fishes; physiological condition; trophic levels.

Coastal upwelling zones are characterized by increased food availability and lowerseawater temperatures (Strub et al., 1998; Poulin et al., 2002a , b; Palumbi, 2003;Narvaez et al., 2004). These are the two most important physical factors linkingoceanographic conditions to the physiology of an organism (Palumbi, 2003). Anincrease in productivity affects key ecological processes, and as many biologicalprocesses are faster in upwelling zones than in non-upwelling zones, this productiv-ity determines the pace of life in coastal communities (Broitman et al., 2001; Mengeet al., 2003; Nielsen & Navarrete, 2004; Pulgar et al., 2011, 2013). High nutrientavailability may in turn determine whether prey (i.e. algae and invertebrates) andtheir consumers display higher physiological performance (Palumbi, 2003). The eco-logical effect of upwelling is in agreement with the food hypothesis, which identifiesquality, availability and predictability of food as important factors capable of modi-fying physiological processes (Cruz-Neto & Bozinovic, 2004). Along this same line,

†Author to whom correspondence should be addressed. Tel.: +56 02 6618416; email: [email protected]

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the ecological and biological evidence of the influence of upwelling indicates a higherphysiological performance in sessile or limited mobility individuals (e.g . limpets,mussels, littorines, barnacles, whelks and keyhole limpets) and a higher growth ratein algae (Dahlhoff & Menge, 1996; Menge, 2000; Menge et al., 2004; Wieters, 2005;Pulgar et al., 2012, 2013). Recent evaluations indicate, however, that in intertidalzones, the upwelling phenomenon is also associated with a nutrient transfer to highertrophic levels, including predators such as fishes. Morphological and molecular evi-dence suggests that the blenny Scartichthys viridis (Valenciennes 1836), an importantherbivore of intertidal communities along the Chilean coast displays greater massgain and biosynthetic capability (estimated as the RNA:DNA) in upwelling thanin non-upwelling zones (Pulgar et al., 2011). The variability in mass gain andbiosynthetic capability may determine differences in the predatory performance (i.e.capture efficiency) when intertidal fishes from upwelling and non-upwelling zonesare compared. The consequences, however, of the physiological variability of inter-tidal vertebrate predators on intertidal community structure and dynamics remainunknown.

The effect of bottom-up control represents an interesting situation as animals con-tinuously cope with environmental fluctuations through behavioural, physiologicaland structural adjustments to ensure appropriate function (Wiener, 1992; Bellardet al., 2012). These adjustments imply that natural selection acts to maximize indi-vidual fitness and that trait combinations are constrained by trade-offs, as explainedby the life-history theory (Fisher, 1930; Roff, 2002). Classic reported trade-offs indi-cate that an increased reproductive effort can enhance reproductive success throughimproved growth and survival, but at the same time, it may compromise adult survival(Hanssen et al., 2005).

Nutrient transfer to herbivorous animals may be predictable because these animalsobtain their food from primary producers, organisms that directly incorporate nutri-ents from their habitat. It is unknown, however, whether the upwelling signals at themorphological or molecular levels are detectable when omnivorous and carnivorousintertidal fishes are analysed. To respond to this question, the several trophic linksthat are in place before nutrient energy reaches these fishes, especially carnivorousones, must be taken into consideration (Lindeman, 1942; Begon et al., 2006).

Understanding the role of upwelling on the nutritional and physiological responsesof fishes representing different trophic levels (herbivores, omnivores and carnivores)is relevant as fishes are the most neglected component of the intertidal fauna,and there is a clear demonstration of their effect on patterns of distribution andabundance of algae and invertebrates (Munoz & Ojeda, 1998; Aldana et al., 2002).Consequently, the variability of the physiological and molecular responses ofintertidal fishes may involve differences in their predatory performance (i.e. captureefficiency and rate of digestive processes), and thus a differential interaction withthe intertidal community may be expected and needs to be re-evaluated (Horn et al.,1999; Pulgar et al., 2011). The aim of this work was to evaluate the morphometricand molecular responses of three fish species, the herbivore S. viridis (Blenniidae),the omnivore Girella laevifrons (Tschudi 1846) (Kyphosidae) and the carnivoreGraus nigra Philippi 1887 (Kyphosidae), from upwelling and non-upwelling zonesin central Chile. Because of methodological limitations, only one species per trophiclevel could be utilized; but the species considered in this study are representative ofthe functional groups to which they belong (Munoz & Ojeda, 1997, 1998; Pulgar

© 2013 The Fisheries Society of the British Isles, Journal of Fish Biology 2013, 83, 1407–1415

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et al., 2005). Considering that energy inputs can strongly influence the rate ofphysiological processes (Menge et al., 2003), it was hypothesized that morphologicaland molecular responses induced by upwelling could be detected in these intertidalspecies.

Two zones on the central Chile coast were studied: one with reported upwelling(U; upwelling, Quintay, 33◦ 11′ S; 71◦ 43′ W) and the other without upwelling (non-upwelling, NU; Las Cruces, 32◦ 00′ S; 71◦ 00′ W) (Wieters et al., 2003; Wieters,2005; Thiel et al., 2007; Pulgar et al., 2011, 2012, 2013). Specimens of the herbiv-orous S. viridis , the omnivorous G. laevifrons and the carnivorous G. nigra wereobtained from tidal pools during austral autumn to winter (A-W) and spring to sum-mer (S-S) seasons and euthanized with an overdose of BZ20 anaesthetic (350 mg l−1).Published gut analyses information was used to perform trophic categorization offishes (Munoz & Ojeda, 1997, 1999; Aldana et al., 2002). All procedures for animalcapture and euthanasia were approved by the Andres Bello University’s BioethicsCommittee.

Two approaches were used to determine fish condition: a morphometric approachwith mass and body size relation comparisons and a molecular approach basedon RNA:DNA determinations. In the morphometric approach, 905 herbivorous (U:n = 523; NU: n = 382), 210 omnivorous (U: n = 179; NU: n = 31) and 185 carniv-orous (U: n = 145; NU: n = 40) fishes were used. The number of animals analysedwas a function of their natural abundance in the field, and these data are coinci-dent with previously reported abundance of the focal species (Hernandez-Miranda &Ojeda, 2006). This indicates that the abundances are representative of the populationstudied; moreover, a similar abundance pattern in both studied zones was observedfor all studied species. Considering published evidence of physiological estimatorsin intertidal fishes, a sample size necessary to compare populations approached 27individuals (Pulgar et al., 2005, 2011). In this study that compares populations intwo study zones and seasons, the sample size exceeds the necessary numbers forthe three species analysed. Moreover, as the sample reflects natural availability ofspecies, the sample size used captures the population variability and also validatesthe statistical analysis. Total fish length (LT) and body mass (M ) were recorded usingcallipers (0·1 cm) and an electronic balance (0·1 g).

In order to standardize ontogenetic development in the samples, for the molecularapproach, only juvenile animals were used and followed the relationship between LTand gut content previously established by Munoz & Ojeda (1997). A total of 101herbivorous (U: n = 57; NU: n = 44), 24 omnivorous (U: n = 12; NU: n = 12) and13 carnivorous (U: n = 9; NU: n = 4) fishes per site were included. Individuals werecaptured and immediately deposited in liquid nitrogen, transported to the laboratoryand kept frozen until analysis. The extraction of RNA and DNA was performed usingTRIzol reagent, as previously described (Pulgar et al., 2011, 2012). After extraction,RNA and DNA were quantified spectrophotometrically and expressed as mg ml−1,with corrections for body and sample size.

In order to avoid a low number of individuals in sampled populations, datafrom seasons with similar environmental conditions were grouped as A-W andS-S. Residual differences in the LT and M relationship and RNA:DNA amongsampled zones and seasons were evaluated using two-way ANOVA. Data wereexamined for assumptions of normality and homogeneity of variance using theKolmogorov–Smirnov and Levene tests. Proportion data were logarithmically


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Table I. General linear model analysis (ANOVA) comparing residuals of total length (LT)and mass (M ) and the RNA:DNA of Scartichthys viridis among study zones and seasons

Effect d.f. MS F P

Residual LT and MStudy zones (Sz) 1 0·62 0·01 >0·05Season (S) 1 878·63 14·14 <0·001Sz × S 1 966·87 15·55 <0·001Error 901 62·15RNA:DNASz 1 1·82 4·04 <0·05S 1 16·07 35·63 <0·001Sz × S 1 0·36 0·80 >0·05Error 97 0·45

transformed. Data are expressed as mean ± s.e. Statistical significance was estab-lished at P < 0·05. All the analyses were performed using General Linear Models(STATISTICA 6.0, StatSoft; www.statsoft.com).

The comparisons of M and LT residuals among upwelling and non-upwelling her-bivorous S. viridis indicate a greater mass gain in relation to body size in upwellingfishes during S-S (Table I and Fig. 1). An a posteriori Tukey (HSD) test showedthat in non-upwelling, S. viridis body size was similar among seasons. In the omniv-orous G. laevifrons , the M and LT residual was higher in the upwelling zone. Whenseasons were considered, however, omnivores showed greater body size during A-W(Table II and Fig. 2). In the carnivorous G. nigra , M and LT residuals were higher inupwelling zones (Table III and Fig. 1), without differences among sampled seasons.RNA:DNA was greater for herbivores in upwelling than in non-upwelling duringS-S, and greater for A-W when compared with the S-S season (Table I and Fig.2).Data for the omnivores indicate higher RNA:DNA in upwelling (Table II and Fig.2). Finally, RNA:DNA was not different for carnivores (Table III).

The results indicate that, in general, upwelling animals would have a higherbiomass than non-upwelling animals. At the molecular level, both herbivorousand omnivorous fishes show signals of the upwelling effect. A greater biomass inupwelling animals is in agreement with evidence obtained from invertebrate species(Chícharo et al., 2001; Palumbi, 2003; Ikeda et al., 2007). A seasonal component inthe morphological response was detected only in the herbivorous and omnivorousspecies; S. viridis displayed higher biomass in S-S and G. laevifrons in A-W(Fig. 1), both in agreement with the strong seasonal influence on food availabilitydescribed for these species (Wieters, 2005). The specific effects of upwelling thatare responsible for this variation are unknown, and this is a relevant question forinvertebrate species, an important source of omnivore food (Munoz & Ojeda, 1997).On the other hand, a higher productivity has been registered in upwelling zones ofcentral Chile (Menge et al., 2004; Wieters, 2005; Pulgar et al., 2011), indicating thatindependent of season, invertebrates grow faster and cover a wider intertidal rocksurface in sectors with upwelling than in similar habitats of a non-upwelling coast(Menge et al., 2003; Palumbi, 2003). The higher biomass observed in upwellingintertidal fishes could be a consequence of an increased exposure to higher nutrient



2

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uals 4

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Fig. 1. Comparison of mass gain in relation to body size (mass, M , and total length, LT, residuals) among(a) Scartichthys viridis , (b) Girella laevifrons and (c) Graus nigra as indicated in upwelling (U, ) andnon-upwelling (NU, ) fishes during the two seasons studied [spring to summer (S-S) and autumn towinter (A-W); *P < 0·05].

availability in upwelling zones compared to non-upwelling zones, which wouldincrease energy in upwelling fishes allowing them to devote resources to othergrowth and reproductive traits (Fisher, 1930). This contention is supported byprevious analyses of limpets and intertidal vertebrates performed in the samelocalities described in this study (Pulgar et al., 2011, 2012, 2013).

RNA:DNA is considered an in situ indicator of the physiological status becauseof its association with the nutritional condition and growth in several marine organ-isms (Buckley & Caldarone, 1999; Chicharo & Chicharo, 2008; Pulgar et al., 2011).Higher RNA:DNA was detected only in species that include algae in their diet(herbivorous and omnivorous), whereas in carnivorous fish, only morphological evi-dence of upwelling effects were observed (Table III). An inability to detect molecularupwelling signals in carnivorous fishes is probably associated with the low number ofanimals analysed and represents one limitation of the study, but does not invalidatethe evidence for upwelling effects.

The implications of different nutrient availabilities for marine animal life historiesare unknown; however, in habitats with low nutrient availability, life-history theorypredicts the presence of a trade-off among life-history traits (Ricklefs & Wikelski,2002; Stearns, 2002; Monaco & Helmuth, 2011). Considering the ‘barrel model’ ofresource allocation (Wiener, 1992), a higher maintenance cost and lower reproduction


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Table II. General linear-model analysis (ANOVA) comparing residuals of total length (LT)and mass (M ) and RNA:DNA of Girella laevifrons among study zones and season

Effect d.f. MS F P

Residual LT and MStudy zones (Sz) 1 171·71 11·84 <0·001Season (S) 1 255·91 17·65 <0·001Sz × S 1 133·26 9·19 <0·01Error 226 14·49RNA:DNASz 1 0·52 8·97 <0·01S 1 0·23 3·93 >0·05Sz × S 1 0·03 0·54 >0·05Error 20 0·06

and growth survival investment (e.g . soft or reproductive tissue) would be predictedin animals from non-upwelling zones.

Interestingly, increased RNA:DNA is related to increased biomass in omnivores,whereas in herbivores, increased RNA:DNA was not associated with an increasein biomass (Figs 1 and 2). As the herbivorous S. viridis inhabits low intertidalpools and the omnivorous G. laevifrons inhabits higher intertidal pools (Pulgaret al., 2005), the variability in physical conditions (i.e. temperature, salinityand oxygen concentration) could be associated with the different physiologicalresponses observed. It is proposed that greater RNA:DNA associated with increasedbiomass in omnivorous fishes is the result of a decreased thermal stress in higherintertidal pools from S-S to A-W seasons, whereas a relatively lower seawatertemperature as a result of upwelling prevents this association in the herbivorous

RN

A:D

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Fig. 2. RNA:DNA among (a) Scartichthys viridis and (b) Girella laevifrons as indicated in upwelling (U, )and non-upwelling (NU, ) fishes during the two seasons studied [spring to summer (S-S) and autumnto winter (A-W); *P < 0·05].



Table III. General linear-model analysis (ANOVA) comparing residuals of total length (LT)and mass (M ) and RNA:DNA of Graus nigra among study zones and season

Effect d.f. MS F P

Residual LT and MStudy zones (Sz) 1 35·87 4·57 <0·05Season (S) 1 0·19 0·024 >0·05Sz × S 1 14·15 1·80 >0·05Error 181 7·84RNA:DNASz 1 0·03 0·63 >0·05S 1 0·15 3·52 >0·05Sz × S 1 0·01 0·19 >0·05Error 9 0·04

S. viridis . This physical variability of habitats (e.g . seawater temperature and nutrientavailability) would promote differential energetic investments of the same genotypeto life-history traits associated with growth and reproduction. The biological effectsof interactions between nutrients and seawater temperature represent unsolvedchallenges to marine eco-physiology.

In this study, only one site per treatment (U v . NU) and only one season’s vari-ation (S-S and A-W) were analysed, which represent one limitation of the study.Nonetheless, the results on spatial and temporal effect of upwelling are in agree-ment with what has been observed at other latitudes (Palumbi, 2003). Moreover, thetwo study zones, Quintay and Las Salinas, have been independently characterizedby other investigators (Broitman et al., 2001; Nielsen & Navarrete, 2004; Wieters,2005) using the same criteria (U v . NU) and, additionally, other studies have recentlyreported U v . NU analyses for intertidal fishes and other taxonomic groups at thesame sites (Pulgar et al., 2011, 2012, 2013). Thus, it is concluded that the presentobservations are not site-specific but can be considered as the expression of spe-cific upwelling-dependent effects on the organism and molecular conditions of therespective intertidal fish species.

This work is the first approach to consider different complexity levels (molecularand individual) of energy transfer in species from different trophic levels, herbivores,omnivores and carnivores, in an important intertidal marine community. More omniv-orous, carnivorous and herbivorous species need to be analysed at the local and geo-graphical scales for a complete trophic level replication. Determining the mechanismsresponsible for this variation in physiological traits and their ecological consequences(Spicer & Gaston, 1999) represent the next steps of continuing investigations.

This study was funded by grants DI17-10R and DI16-12R of the Andres Bello Universityto J.P. and by the Central University’s grant to M.A.

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can upwelling signals be detected in intertidal fishes of different trophic levels?

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