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Acta Oecologica 41 (2012) 58e64

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Acta Oecologica

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Original article

Variability of Lekanesphaera monodi metabolic rates with habitat trophic status

Fabio Vignes a,*, Marialaura Fedele a, Maurizio Pinna a, Giorgio Mancinelli a, Alberto Basset a,b

aDept. of Biological and Environmental Science and Technology, University of the Salento, Via Prov.le Lecce-Monteroni, 73100 Lecce, Italyb Istituto di Biomembrane e Bioenergetica (IBBE), Via G. Amendola 165/A, 70126 Bari, Italy

a r t i c l e i n f o

Article history:Received 4 January 2012Accepted 14 April 2012Available online

Keywords:Standard metabolic rateBody condition indexTransitional water ecosystemsTrophic statusFood habits hypothesis

* Corresponding author. Tel.: þ390832298600; fax:E-mail address: fabio.vignes@unisalento.it (F. Vign

1146-609X/$ e see front matter � 2012 Published bydoi:10.1016/j.actao.2012.04.006

a b s t r a c t

Regulation of metabolism is a common strategy used by individuals to respond to a changing environ-ment. The mechanisms underlying the variability of metabolic rates in macroinvertebrates are of primaryimportance in studying benthicepelagic energy transfer in transitional water ecosystems.

Lekanesphaera monodi is an isopod endemic to transitional water ecosystems that can modify itsmetabolic rate in response to environmental changes. Therefore it is a useful model in studying theinfluence of environmental factors on metabolism.

This study focused on the interpopulation variability of standard metabolic rates (SMR) in L. monodipopulations sampled in three transitional water ecosystems differing in their trophic status. The standardmetabolic rates of L. monodi individuals across the same range of body size spectra were inferred fromoxygen consumption measurements in a flow-through respirometer in the three populations and a bodycondition index was assessed for each population. Habitat trophic status was evaluated by monthlymeasurement of the basic physicalechemical parameters of the water column in the ecosystems for oneyear.

Standard metabolic rates showed high variability, ranging from 0.27 to 10.14 J d�1. Body size accountedfor more than 38% of total variability. In terms of trophic status, individuals from the eutrophic ecosystemhad significantly higher standard metabolic rates than individuals from the other ecosystems(SMR ¼ 2.3 J d�1 in Spunderati Sud vs. 1.36 J d�1 in Alimini and 0.69 J d�1 in Acquatina). The bodyconditions index was also higher in the population from the eutrophic ecosystem.

Results show that standard metabolic rates and growth rates are directly related to habitat produc-tivity in accordance with the expectations of the food habits hypothesis. A possible extension of thishypothesis to benthic invertebrates is proposed.

� 2012 Published by Elsevier Masson SAS.

1. Introduction

The metabolism of benthic invertebrates is influenced by bothphysiological factors (body size, activity, daily rhythms) and envi-ronmental factors (temperature, oxygen concentration, food avail-ability, competition) (Allan et al., 2006; Lampert, 1984). Everyenvironmental change requires the individual to reallocate energyas part of the acclimation process (principle of allocation;MacArthur and Levins, 1964). This process involves an adjustmentof physiological processes which, in turn, has a metabolic cost.

Transitional water ecosystems are characterized by frequent andsudden variations in abiotic factors that force animals to modifytheir energy-consumption strategies. This usually induces higherrespiration rates with increased metabolic expenditure. Several

þ390832298722.es).

Elsevier Masson SAS.

authors have described an increase in invertebrate respiration rateswith variations in single environmental factors. The effect of short-term and prolonged temperature fluctuations was described byNewell (1969), who found marked variations in respirationrates during short-term fluctuations and an inverse relationshipwith temperature in long-term or seasonal fluctuations. Otherstudies report a linear increase in respiration rates with tempera-ture in various Idotea species (Salomon and Buchholz, 2000; Vetteret al., 1999), Asellus aquaticus (Adcock, 1982) and Trichoniscuspusillus (Meyer and Phillipson, 1983). Allan et al. (2006) describedincreased respiration rates in Palaemon peringueyi over a salinityrange of 5e45 ppt. Hoback and Barnhart (1996) observed a curvi-linear direct relationship between respiration rates and dissolvedoxygen concentrations in Gammarus pseudolimnaeus. Traceelements (As, Cd, Cr, Cu, Se) were found to produce increasedmetabolic costs in Procambarus acutus (Rowe et al., 2001). Dis-solved nutrients and suspended primary producers were seen tohave an effect on food availability for deposit feeders in transitional

F. Vignes et al. / Acta Oecologica 41 (2012) 58e64 59

water ecosystems (Pakulski et al., 2000). Newell (1973) reportedthat in intertidal organisms, environmental factors normally asso-ciated with the presence of food may induce higher levels ofactivity, with an increased respiration rate. Bayne et al. (1989) andThompson and Bayne (1972) showed that the presence of partic-ulate food in water induced an increase in the respiration rates ofbivalves. However, the complexity and interdependence of many ofthe factors which influence the respiration of intertidal organismswas well recognised (Newell, 1973). In transitional water ecosys-tems, several environmental factors fluctuate at the same time,synergistically influencing the overall trophic status of theecosystem as is usually the case with eutrophication (Vignes et al.,2009). By itself, the trophic status seems to be a suitable integrativefactor that, can in turn, influence important ecological processessuch as primary productivity and decomposition as well asa number of abiotic factors including oxygen concentration,nutrient release mechanisms, seston concentration, and others(Basset et al., in press).

An explanation of how environmental productivity can affectmetabolism is the food habit hypothesis (FHH;McNab,1986), whichpredicts that the mass-independent Basal Metabolic Rate (BMR) inendotherms is associatedwith dietary traits. In accordancewith thishypothesis Cruz-Neto and Jones (2005) and McNab (2002) statedthat low mass-independent Basal Metabolic Rates (BMR) are likelyto occur in habitats where food availability is poor, low in quality orunpredictable. The evidence underlying the FHHcomesmainly frominterspecific studies on mammals (Bozinovic et al., 2007).

In spite of decades of research, this hypothesis remainscontroversial due to doubt about the relative importance of dietquality in interspecific comparisons (Cruz-Neto et al., 2001; McNab,2002) and differences in body size, seasonality and experimentalprocedures (Bozinovic et al., 2007). Bozinovic et al. (2007) high-lighted the need for intraspecific or intrapopulation comparisons inorder to compensate for these pitfalls. Studies comparing differentpopulations of the same species could shed light on how differ-ences in physiological traits evolve and are affected by ecologicaland environmental factors. Although the food habits hypothesis hasbeen extensively studied in vertebrates, few attempts have beenmade to extend this hypothesis on invertebrates. Nowadays littleinformation is available on the relationship between habitattrophic status and the metabolic response of benthic macrofauna.An intraspecific comparative study, testing populations living indifferent habitats in the same geographical region, should providean effective tool for understanding the adaptive value of physio-logical trait variability, and its consequences in terms of the foodhabits hypothesis among benthic invertebrates.

The aim of the present study was to determine how differenttrophic status influences metabolic rates in comparable pop-ulations of the isopod Lekanesphaera monodi living in three tran-sitional water ecosystems. The relationship between variations inmetabolic rates and a body condition index which measures theforaging success and ultimately the fitness of animals in these

Table 1Average values � standard deviations and ranges of variations of physical and chemicainorganic nitrogen; TP ¼ total phosphorous; Chla ¼ Chlorophyll a; DO ¼ dissolved oxyge

Acquatina Alimini

Mean � SD Range Mean � SD

Temperature (�C) 16.5 � 5.7 8.8e25.3 19.3 � 5.Salinity (&) 31.5 � 5.3 20.5e38.0 26.5 � 4.DIN (mg l�1) 95.9 � 57.2 35.0e616.0 199.3 � 96TP (mg l�1) 1.7 � 1.4 0e3.1 7.8 � 6.D.O. (%) 99 � 17 82e122 96Chla (mg l�1) 1.7 � 0.7 0.1e5.1 5.0 � 3.TRIX 4.9 6.1

particular ecosystems (Basset, 1993; Basset and Glazier, 1995) wasalso explored.

2. Materials and methods

2.1. Study organism

L. monodiwas used as a model species. It is an isopod belongingto the Sphaeromatidae family. It is strongly endemic to southernItalian lagoons and this endemism is potentially highly informativein biogeographical analyses. This species lives in habitats withhighly variable physicalechemical conditions, modulating itsmetabolic processes in response to environmental changes. It iswidespread in southern Italian lagoons and is thought to play animportant role in benthicepelagic coupling in these systems(Jansen, 1971). Due to its abundance and long life cycle in thebenthic compartment it may also be considered a useful ecologicalindicator in transitional water systems.

In order to exclude the effects on metabolic rates of othervariables (such as climate, season, body size range, developmentalstage and experimental protocol), all specimens were sampled inthe same period (the first twoweeks of June) using a hand operatedsampler (0.5 mm mesh) in each aquatic ecosystem. Dense pop-ulations of L. monodi were usually found among macrophytes andbottom organic detritus. Specimens of L. monodi were carefullyselected immediately in the field. The isopods were then placed ina refrigerated box containing natural water and transferred to theEcology Laboratory at the University of the Salento as soon aspossible. Body length and dry mass weremeasured on a populationof approximately 200 specimens from each ecosystem. A sub-sample of 20 male individuals 3e13 mm in length were thenselected with the help of a stereomicroscope, transferred to artifi-cial pond water (APW; Naylor et al., 1989) in aerated aquaria at15 � 0.5 �C and kept unfed for at least 24e33 h before measuringthe respiratory rate.

2.2. Habitat of origin

This study was carried out in three transitional water ecosys-tems located in southern Italy (Acquatina, Alimini and SpunderatiSud) with differing trophic states. They were selected, at firstglance, on the basis of subjective visual in situ observations (ofwater turbidity, algal blooms, sediment organic matter, submergedmacrophytes and macroalgal vegetation). Two (Acquatina and Ali-mini) were found to suffer from very limited anthropic impacts,consisting mainly of extensive fish-farming. Spunderati Sud,receives waste-waters from an intensive fish-farm. Trophic statuswas determined by monthly evaluation of dissolved inorganicnutrients, oxygen concentration and phytoplankton biomassmeasured as chlorophyll a (Table 1) and summarized with theintegrated TRIX index (Vollenweider et al., 1998).

l parameters and primary producer biomass in three ecosystems (DIN ¼ dissolvedn).

Spunderati Sud

Range Mean � SD Range

6 10.7e28.4 20.1 � 6.2 12.8e28.87 16.5e35.8 32.8 � 4.1 23.0e38.7.3 0e634.8 1464.5 � 1010.5 268.5e12914.35 0e24.9 69.7 � 41.0 6.7e166.6

79e113 89 68e1151 0.1e25.2 10.6 � 5.2 1.3e21.1

7.9

F. Vignes et al. / Acta Oecologica 41 (2012) 58e6460

2.2.1. AcquatinaAcquatina (N 40�260 4200; E 18�140 1000 e Area: 0.45 km2 e mean

depth 1.2 m) is a man-made basin receiving continuous input offreshwater from a drainage channel and is permanently connectedto the Adriatic Sea by a large artificial channel. The substrate ismainly composed of mud and, in a few locations, rocks. At the timeof the study it was being exploited for experimental marine aqua-culture. Previous studies of nutrient concentration and primaryproducer biomass allow Acquatina to be considered an oligotrophicbasin (Fiocca et al., 1998).

2.2.2. AliminiAlimini (N 40�120 1000; E 18�260 5000 e Area: 1.375 km2 e mean

depth 1.5 m) is a natural lagoon. It collects freshwater from thesurroundings by means of a drainage channel and from a fresh-water lake to the south and is permanently connected to theAdriatic Sea through an artificial inlet. The substrate is mainlycomposed of mud with local accumulation of riparian vegetationdetritus. Nutrient content and primary producer biomass aretypical of a mesotrophic system (Vignes et al., 1999).

2.2.3. Spunderati SudSpunderati Sud (N 39� 510 1200; E 18� 100 2500 e Area 0.145 km2 e

mean depth 1.2 m): is the southernmost basin of an artificialcomplex of seven basins. It is connected to the Ionian Sea througha short artificial channel and directly receives waste water froman intensive fish-farm. Due to its richness in nutrients andorganic matter, this system is considered eutrophic (Basset et al.,2003).

2.3. Methods

The habitat trophic status of the three transitional waterecosystems was evaluated by means of the TRIX index(Vollenweider et al., 1998) in accordance with the followingformula:

TRIX ¼ ½Log10ðChlaÞ þ Log10ð%DOÞ þ Log10ðDINÞ þ Log10ðTPÞ� ð�kÞ�=m

Oxygen concentration (%DO) was measured in situ by means ofa multiparametric probe. Dissolved nutrients (DIN, TP) weredetermined by spectrophotometric methods as reported byStrickland and Parsons (1968) with minor modifications. Phyto-plankton biomass (Chla) was determined as chlorophyll a bya spectrofluorimetric method (Yentsch and Menzel, 1963) on 90%acetone extracts. The parameters k and m in the formula are scalecoefficients (1.5 and 1.2, respectively), introduced in order to set thelower limit of the Trophic Scale to 0 and the upper limit to 10 TRIXunits.

The body condition index of L. monodi specimens was estimatedfrom the ratio between measured and expected body mass, thelatter being inferred from the relationship between body lengthand body size mass in 600 individuals pooled from all threeecosystems (Jakob et al., 1996). Individual body length wasmeasured to the nearest 0.01 mm from the base of the antennae tothe end of the telson, by means of an image analysis system (LeicaQWIN 3) using a stereomicroscope (Leica MZ12, 12� magnifica-tion). Individual body mass was measured with a Sartorius MC5microbalance to the nearest�0.001mg, after drying in a 60 �C ovenfor at least 3 days. Finally Ash Free Dry Weight (AFDW) wasdetermined after ignition in a muffle furnace for 6 h at 500 �C(Payne, 1970). AFDW, obtained by subtracting the ash content(61e64% of total dry mass), was considered to offer a bettercomparison with other detritivores than dry weight.

To take account of the influence of body mass on respirationrates in sub-samples, the highest range of body length that allowedfor comparison across all three ecosystems was chosen. Respirationrates were measured individually for specimens with body lengthsof 3e13 mm by means of a flow-through respirometer using 5 mlglass syringes as respiration chambers and a Clarke-type micro-electrode (Strathkelvin 781b) as a detector. All experiments wereconducted in a thermostatically regulated room at 15� 0.5 �C usingAPW as an incubation medium. APW was prepared and kept in thethermostatic room to prevent any temperature change. Animalswere kept unfed in APW aquaria for at least 12e18 h before theirtransfer to respirometric chambers. Each glass syringe was flushedwith APWat a finely regulated flow rate of approximately 5 ml h�1.Animals remained closed for 12e15 h (equilibration time) beforereadings. The equilibration time was calculated following Lampert(1984) as the time required to reach a steady state of dissolvedoxygen concentration in the experimental equipment. The equili-bration time depended on system flushing characteristics, chambervolume, mean animal size and flow rate. The isopods rapidlybecame inactive during the equilibration period. The total starva-tion time varied from 24 to 33 h. This time was considered suffi-cient to exclude any of Specific Dynamic Action (SDA), which in thisspecies was timed at 23 � 1.5 h. The oxygen consumed by eachindividual was estimated by calculating the difference between thefinal dissolved oxygen concentration at the end of the incubationperiod and the oxygen concentration, near full saturation, in theAPW flowing into each experimental chamber. Oxygen uptakevalues were transformed to energy equivalents (J d�1) in accor-dance with Wilkes and McMahon (1982) as reported in Basset(1990). Individual respiration rates were, also expressed on a per-weight basis by dividing by individual AFDW.

2.4. Data analysis

A general allometric equation in the form of Y¼a*Xbwas used todescribe the relationships between body length and body mass andbetween respiration rates and dry tissue weight. Specifically, thecorrelation of body mass with body length was assessed withreference toW ¼ a*Lb, where “W” is the individual AFDW, “L” is theindividual length, constant “b” is the length exponent and “a” is theAFDW for an individual of 1 mm in length. In the same way, themodel used to describe the dependence of respiration rate on bodymass was RR ¼ a*AFDWb where RR is the individual respirationrate, constant “b” is the weight exponent and “a” is the rate for anindividual of 1 g dry mass.

One Way ANOVA was performed to test differences in meanvalues among environmental conditions at the three ecosystems.

Respiration rates among populations were compared usinglogarithmic transformed data in order to linearize the relationshipwith body mass and to meet model assumptions of normality ofmodel residuals and homogeneity of variance. For analysis ofcovariance (ANCOVA), we checked for parallelism and elevationsusing a test for interaction with the covariate (i.e. body mass)following Zar (1984). A Bonferroni’s multiple comparison post testwas used to compare groups. Biotic condition indexes were alsotested by ANCOVA.

A probability of a ¼ 5% was selected to guard against falselyaccepting a null hypothesis.

3. Results

3.1. Trophic state of habitat

Table 1 lists the main environmental parameters and theirranges over an annual period. Temperature, salinity and dissolved

0:01

Fig. 2. Relationship between Y-intercept (�SD) of regression line in each populationand TRIX of each ecosystem.

F. Vignes et al. / Acta Oecologica 41 (2012) 58e64 61

oxygen in the three ecosystems were not found to be significantlydifferent (one way ANOVA P > 0.05), probably due to the shal-lowness of the three ecosystems which were exposed to basicallysimilar meteorological conditions. In contrast nutrient concentra-tions and chlorophyll content were found to be very different (oneway ANOVA P < 0.05). The TRIX values, based on the annualchemical and biological data set, showed that the ecosystems withthe highest trophic status was Spunderati Sud (TRIX ¼ 7.9), fol-lowed by Alimini (TRIX¼ 6.1) and then Acquatina (TRIX¼ 4.9). Thisconfirmed our preliminary assumptions about the trophic status ofthe three ecosystems.

3.2. Standard metabolic rates

The individual standard metabolic rates of L. monodi rangedfrom 0.27 to 10.14 J d�1. They showed a strongly asymmetricfrequency distribution with a median of 2.86 J d�1. More than 88%of the entire data set was below 6.0 J d�1. The weight-specificrespiration rates of L. monodi individuals ranged from 0.09 to2.88 J d�1 mg�1 with a median value of 0.43 J d�1 mg�1, and morethan 90% of the entire data set was below 2.0 J d�1 mg�1.

3.3. Effect of body size

The AFDW of L. monodi individuals in sub-samples taken forrespirometry measurements ranged from 0.14 to 19.63 mg. Indi-vidual respiratory rate and AFDW were found to be allometricallycorrelated, and the relationship was significantly described by thefollowing regression equation:

SMR ¼ 1:15*AFDW0:46ðr ¼ 0:62 p < 0:01Þ:AFDW explained 38% of the total variability, increasing to 46%

when the above relationship was converted to weight-specificvalues by normalizing the individual respiration rates for indi-vidual biomass (weight-specific respiration rate). In this case thebest fitting equation was the following:

SMR ¼ 1:14*AFDW�0:54ðr ¼ �0:68 p < 0:01Þ:As expected, higher weight-specific oxygen consumption is

observed in smaller individuals.

3.4. Effect of habitat trophic status

Body size was always significantly related to SMR. The weight-specific respiration rates of each L. monodi population, plotted ona double logarithmic graph (Fig. 1), returned the followingequations:

Fig. 1. Comparison of regression lines between weight-specific SMR and body mass inthree populations. Statistical details in Results (par. 3.4).

Acquatina : SMR ¼ 0:69*AFDW�0:53 r ¼ �0:90 P < 0:01Alimini : SMR ¼ 1:36*AFDW�0:65 r ¼ �0:76 P < 0:01Spunderati Sud : SMR ¼ 2:31*AFDW�0:64 r ¼ �0:78 P <

The slopes of exponential regression lines among the threepopulation were found to be not significantly different (ANCOVAF ¼ 0.51, P > 0.05), but differences in elevations were found to behighly significant (F ¼ 22.89, P < 0.01), showing differences inweight-specific respiration rates among populations across thewhole size range.

The relationship between trophic status, as indicated by theTRIX index, and the regression line intercepts (i.e. respiration ratesper unit of biomass) presented a linear trend as shown in Fig. 2.

3.5. Body condition index

The body condition index was calculated as the ratio betweenmeasured and expected body mass. Length ranged from 1.10 mm to13.00 mm, while measured body mass varied between 0.085 and25.392 mg. As a whole, the relationship between body length andAFDW was best described by the model.

W ¼ 0:06*L2:37ðr ¼ 0:91; P < 0:01Þ:When populations were considered separately, analysis of

variance showed a significant differences (P < 0.01) in the bodycondition indices of the three populations (Fig. 3), with higherindex values for populations living in more trophic ecosystems.

Fig. 3. Distributions of body condition indices among three populations.

F. Vignes et al. / Acta Oecologica 41 (2012) 58e6462

A Bonferroni’s multiple comparison post test also revealed signifi-cant differences for all combinations (P < 0.01).

4. Discussion

A number of studies have investigated the relationshipbetween mass-independent SMR and environmental factors ininvertebrates. Most of these have focused on temperature andwater salinity (Allan et al., 2006). Moreover a strong associationwith food availability and/or predictability has been recognized inendotherms (Bozinovic et al., 2009; McNab, 2002). The availableinformation on the dependence of SMR on habitat productivity ininvertebrates is very limited. Our study shows a close relationshipbetween the mass-independent SMR of an isopod species andhabitat trophic status. As expected body mass as AFDW wasobserved to exert a strong influence on standard metabolic rates(West et al., 1997), accounting for more than 38% of overallintraspecific variability. Part of the large residual variation appearsto be explained by the trophic status of the original habitat. Inspite of the acclimation period under laboratory conditions, therewere significant differences in interpopulation standard metabolicrates. The intrapopulation relationships between weight-specificmetabolic rates and body mass had significantly higher coeffi-cients of determination, varying from 58% to 81%. The threeregression lines were found to be parallel but the elevations weresignificantly different from each other. This implies a similarpattern of standard metabolic rates scaling with body size insideeach population but different energy consumption per mass unitacross the entire size spectrum, with animals from Spunderati Sudconsuming, on average, more than three times as much as thosefrom Acquatina. These observations cannot be explained withreference to differences in physical factors such as temperature,dissolved oxygen or salinity since we measured high andcomparable ranges of variation throughout the year in all threeecosystems. Indeed, chemical factors such as dissolved nutrientsand chlorophyll a concentration were significantly differentamong the three ecosystems, although they covaried. Most ofthese chemical factors are correlated with primary productivityand ultimately food availability in aquatic ecosystems. In transi-tional water systems, most of the newly produced organic matterenters the detritus food chain. Hence, at least for detritivoresspecies, high ecosystem productivity should reflect high foodavailability, although productivity and food availability varyamong differing habitats in complex ways.

A rise in trophic status, as frequently occurs in transitional watersystems being characterised by high vigour and exergy content(Basset et al., in press), could be perceived by organisms either asa stress factor that forces them to modify their physiologicalprocesses or as an increase in resource availability, helping toincrease their fitness. An increase in metabolic rates subsequent toa rise in trophic status, in order to counterbalance the degradationof environmental conditions, has been widely demonstrated(Koehn and Bayne, 1989). In this scenario, the displacement ofenergy to counterbalance the disturbance should reduce secondaryproduction. On the other hand, if an increase in habitat productivityresulting from higher trophic status leads to greater energy avail-ability or food predictability, it can represent an advantage for somespecies, giving them a competitive edge over others. In thisscenario, since standard metabolic rates regulate the conversion ofassimilated energy into new body tissue, the expected result is anincrease in secondary production both as body condition index andas fitness. In our study the converging trends of increased bodycondition index and standard metabolic rates with habitat trophicstatus indicate that L. monodi benefits from greater habitatproductivity (Fig. 3).

This observation is consistent with previous studies by Muellerand Diamond (2001), who found a direct relationship between nethabitat primary production and basal metabolic rates of differentPeromyscus species, and by Bayne et al. (1989), who found anincrease in the respiratory rates of Mytilus edulis in response toincreased food availability.

Our evidence seems to agree with the prediction of the Foodhabits hypothesis, even though this hypothesis was developed fora phylogenetically distant group (McNab, 1988). Assuming thatenergy constraints act as a common denominator at any taxonomiclevel, we hypothesized that the increase in energy or food avail-ability could also raise metabolic and production rates in phylo-genetically lower taxonomic categories such as invertebrates. Toour knowledge this is the first study testing the food habitshypothesis in benthic macroinvertebrates under field conditions,although no attempt was made to distinguish between the threecomponents that can influence SMR (food availability, quality andpredictability; Bozinovic et al., 2007).

The mechanisms involved in population responses to trophicstatus change were not investigated in this study. Higher metabolicrates have been interpreted as advantageous in ectotherms becausethey enable them tometabolize foodmore rapidly, to develop fasterand thus to complete their life cycle in a shorter period of time(Chown and Gaston, 1999). However Clarke (1993) argues that foriteroparous organisms, metabolism represents a cost, not a benefit,because elevated metabolic rates impose higher costs on growthand development. L. monodi is considered an iteroparous speciesand, in southern Italian lagoons, often achieves two reproductiveevents, in early spring and late summer (personal observation). Anincrease in the metabolic rate could help to fulfil this goal.

Conversely, lower total metabolic costs in oligotrophic habitatsmight therefore be an adequate adaptive strategy to decreaseenergy loss in environments with low resource levels (Mueller andDiamond, 2001).

When benthic macroinvertebrates are exposed to long-termchanges in habitat trophic status they can obtain optimal perfor-mance by altering their metabolism, either by phenotypic plasticityor genetic adaptation.

Local adaptations play a crucial role in generating phenotypicand population divergence (Turelli et al., 2001). Guderley and Blier(1988) suggested that differences in metabolic rate between pop-ulations of a single fish species reflect adaptations to specificenvironmental conditions. In broadly distributed ectothermspecies, intraspecific clinal patterns of variation are frequentlyattributed to natural selection, and hence are presumed to reflectgenetic adaptation to local conditions (Alatalo and Gustafson, 1988;Lardies and Bozinovic, 2008; Mousseau and Roff, 1989). Severalstudies have pointed out that a significant genetic contribution tovariation in individual energy budgets is often spatially or tempo-rally correlated with variation in environmental factors and whole-animal physiological processes (Mitton et al., 1986; Pujolar et al.,2005; Teska et al., 1990). In our study the three populations werephysically separated from each other and in this case changes inenvironmental conditions can alter genetic composition in a veryshort period of time.

On the other hand geographical variation is not in itself proof ofnatural selection because metabolic traits can vary due to pheno-typic plasticity, which allows the organisms to cope with fluctu-ating and unpredictable environments in an ecological time scalewithout leading to changes in genotype (Stearns, 1989) or micro-evolutionary processes (Hansen and Boonstra, 2000). Sabat et al.(2004) proposed that the ability to modify the phenotype inresponse to environmental cues might be higher in species orpopulations that experience major changes in environmentalvariables (e.g., temperature) than in those that rarely experience

F. Vignes et al. / Acta Oecologica 41 (2012) 58e64 63

extreme environmental fluctuations. Our data do not allow settle-ment of the question and further laboratory-based cross acclima-tion studies should help to resolve this issue.

In addition, differentiation in standard metabolic rates caninfluence resource exploitation behaviour. SMR may vary acrossspace in a predictable way, as a function of variation in thoseecological conditions that affect food intake rates. When food isabundant, individuals with high SMR may benefit by being able toengage in high levels of energetically costly behaviour, and/or highrates of biomass production. This shift in metabolic rate may alsodetermine shifts in trophic niche width (Basset and Rossi, 1990;Roughgarden, 1979; Schoener, 1969), in the range of distribution ofanimals (Bozinovic and Rosenmann, 1989; McNab, 1988) and in thespecialist/generalist ratio within each population (Rossi, 1985).

The mechanisms by which metabolism increases with envi-ronmental trophic status could affect processes at the ecosystemlevel. Indeed, benthic macroinvertebrates are the point of contactbetween the grazing food chain and the detritus food chain and arecrucial to the regulation of decomposition rates, nitrogen andphosphorusmobilization and energy transfer coupling. Variation inabundance, productivity or species relationships at this level couldseriously disrupt the higher trophic levels. Additionally the increasein metabolism with trophic status could potentially change thetrophic transfer efficiency. This effect should be considered also inecotrophic modelling of transitional water ecosystems whichshould also take into account for variation in ecotrophic efficiencyof species assemblages with changing in physical environment andhabitat (Neira et al., 2004; Christensen et al., 1996). The increasedmetabolic rates and body condition index in L. monodi also need tobe examined in terms of the variation in the species’ interactionwith competitors. These aspectsdeserve closerattention; significantefforts are required to understand the effects of eutrophication ondetritivore metabolism.

5. Conclusion

In summary, we found that SMR and body mass differ amongthree populations of L. monodi living in three habitats with differenttrophic status. Both SMR and BCI change linearly in the differenthabitats. The evident correlation between SMR and BCI can beexplained with reference to the food habits hypothesis andsuggests a possible extension of this theory to benthic invertebratepopulations. Changes in metabolic rates may be due to bothevolutionary and phenotypic adaptations. Our results do not allowus to discriminate between the two phenomena, although otherstudies comparing geographically segregated populations stronglysuggest the existence of local genetically based differentiation.However we cannot exclude the effect of developmental plasticityin our case.

Acknowledegments

This research was financially supported by PRIN 2008 (Projectsfor Research of National Interest), and by the Italian Ministry ofUniversity and Research (MIUR). We also thank two anonymousreferees for their comments and suggestions for an earlier draft ofthis paper.

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