Food, feeding and growth rates of peracarid macro-decomposers in a Ria Formosa salt marsh, southern Portugal

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Journal of Experimental Marine Biolo

Food, feeding and growth rates of peracarid macro-decomposers

in a Ria Formosa salt marsh, southern Portugal

Natalia Diasa,b,*, Mark Hassallb

aUniversidade do Algarve, Faculdade de Ciencias do Mar e do Ambiente, Campus de Gambelas, P-8005-139, Faro, PortugalbCentre for Ecology Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich,

NR4 7TJ, United Kingdom

Received 28 September 2004; received in revised form 27 April 2005; accepted 29 April 2005

Abstract

The diet, feeding rates and growth rates of three species of isopod and three species of amphipod from a Ria Formosa salt

marsh in southern Portugal are compared to test the hypotheses that the relative success of amphipods as macro-decomposers in

salt marshes worldwide can be a) attributed to their utilizing a distinctly different range of potentially available food resources

and b) attributed to them using similar food resources but at different rates.

The first hypothesis was tested using a combination of gut contents analysis, stable isotope analysis and multiple-choice food

preference tests. The results of all three analyses showed that there was a very broad overlap in the resource utilization curves for

these species for the most abundant potential foods available in the upper salt marsh. The first hypothesis was therefore rejected.

The second hypothesis was tested with palatability experiments in which consumption rates of each of the test animals were

compared for each potential food offered alone. The amphipods ate all five of the foods significantly faster, consuming from 3–

73� more food per unit mass than the isopods.

Analyses of their relative growth rates from when released from the marsupium until first breeding, showed that amphipods

have a faster growth rate than isopods in the field which is consistent with other traits in their rapid development–high fecundity

life–history strategy. We conclude that these data support the second hypothesis and that their morphological adaptations to a

shredding, high ingestion-rate rapid gut turnover digestive strategy enable them to have a more efficient resource acquisition

rate than the slower growing, lower fecundity and slower ingestion-rate longer gut throughput time strategy of most isopods.

D 2005 Elsevier B.V. All rights reserved.

Keywords: Amphipod; Consumption rates; Food preferences; Gut contents; Isopod; Stable isotopes

0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.jembe.2005.04.017

* Corresponding author. Centre for Ecology Evolution and Con-

servation, School of Environmental Sciences, University of East

Anglia, Norwich, NR4 7TJ, United Kingdom. Tel.: +44 1603591426;

fax: +44 1603591327.

E-mail address: [email protected] (N. Dias).

1. Introduction

Primary production in salt marshes is often very

high (Odum, 1970; Chapman, 1992; Vernberg, 1993)

but consumption by herbivores is extremely limited

gy and Ecology 325 (2005) 84–94

N. Dias, M. Hassall / J. Exp. Mar. Biol. Ecol. 325 (2005) 84–94 85

(e.g., Jackson et al., 1985; Daehler and Strong, 1995;

Packham and Willis, 1997; Pennings and Bertness,

2001), and most of the biomass of the marsh vege-

tation passes through the detritus pathway which

includes a high range of macro- and microoganisms

(Duarte and Cebrian, 1996; Hemminga et al., 1996;

Packham and Willis, 1997; Pennings and Bertness,

2001). Salt marshes are, however, also highly stress-

ful environments which are subject to high fluctua-

tions in temperature, moisture content and osmotic

pressures. Typically, relatively few species of inver-

tebrates adapt to such conditions but those which

have done so can reach extremely high population

densities (Montague et al., 1981; Chapman, 1992;

Levin and Talley, 2000).

The Peracarida includes some very successful salt

marsh species, particularly amongst members of the

Amphipoda which are widespread and abundant in

many salt marshes (Dahal, 1952; Averill, 1976;

Robertson and Lucas, 1983; Stenton-Dozey and Grif-

fiths, 1983; Inglis, 1989), usually more so than mem-

bers of the Isopoda which are better adapted than most

amphipods to fully terrestrial habitats (Sutton, 1980).

One reason for the difference in the extent to which

they are adapted to the salt marsh habitat might be that

amphipods are able to utilize a wider range of foods

potentially available in salt marsh habitats. Another

possible reason could be that they utilize the same

foods but more effectively.

We test these two hypotheses for amphipods and

isopods which co-exist in a Ria Formosa salt marsh

in southern Portugal (Dias and Hassall, in press-a) by

applying a range of methods of diet analysis, includ-

ing food preference tests, gut contents analysis and

stable isotope analysis and by measuring consump-

tion rates on diets of different potential foods. The

Table 1

Characteristics of the isopod and amphipod species in the Ria Formosa sa

Micro-habitat occupied M

l

Tylos ponticus Burrows in the sand 1

Porcellio lamellatus Under wrack 1

Halophiloscia couchii Under wrack 1

Orchestia gammarellus Under wrack 1

Orchestia mediterranea Under wrack 2

Talorchestia deshayesii Burrows in the sand 1

a Source: Louis (1980).

relative success of the observed resource utilization

strategies is then evaluated by comparing growth

rates for these species in the field. The conclusions

drawn are then interpreted in relation to differences

in alimentary morphology between the two orders

and the consequences for their resource allocation

strategies.

2. Material and methods

2.1. Sample collection

Samples were collected by hand from the upper

fringe of a Ria Formosa lagoon salt marsh (southern

Portugal) (378 00V N, 078 59V W). The salt marshes in

this lagoon are of the dry-coast type (Adam, 1990)

with the vegetation consisting of Spartina maritima

(Curtis) Fernald in the lower level, Sarcocornia spp.

and Atriplex portulacoides L. in the intermediate

region, and Suaeda vera J. F. Gmelin, Suaeda mar-

itima (L.) Dumort, Atriplex halimus L., and Limonias-

trum monoptalum (L.) Bss. in the upper zone. Six

peracarid species inhabiting the superior marsh have

been studied: three isopods: Tylos ponticus Greb-

nitzky, 1874 (Tylidae), Porcellio lamellatus Budde-

Lund, 1879 (Porcellionidae) and Halophiloscia cou-

chii (Kinahan, 1858) (Halophilosciidae); and three

amphipods: Orchestia gammarellus (Pallas, 1766)

(Talitridae), Orchestia mediterranea A. Costa, 1857

(Talitridae) and Talorchestia deshayesii (Audouin,

1826) (Talitridae) (Table 1). Other aspects of the

ecology and secondary production of these macro-

decomposers have been reported elsewhere (Dias,

2002, 2003; Dias and Sprung, 2003, 2004; Dias and

Hassall, in press-a).

lt marsh

aximum

ength (mm)

Reproductive

period

Mean density

(ind. m�2)

4 May–Sep/Oct 2950

4 March–Sep/Oct 36

1 March–Sep/Oct 3

6 Year round 358

6 Year round 46

1 March–Nova 43

N. Dias, M. Hassall / J. Exp. Mar. Biol. Ecol. 325 (2005) 84–9486

2.2. Gut content analysis

Animals used for gut content analysis were frozen,

and then dissected under a binocular microscope. The

digestive tracts were placed on a flat surface and the

contents of the whole digestive tract observed under

an optical microscope. Fifty digestive tracts from

adult females and males of each of the 6 species

were collected in the summer and analysed. Zostera

noltii Hornem, S. maritima, diatoms, green algae

(plant tissues and fragments of filamentous algae)

were identified by comparison with preparations of

relevant materials collected at the sampling site. The

relative percentage of each was estimated according to

the area occupied. All other materials were classified

as undetermined vegetable detritus.

2.3. Stable isotope analysis

Samples of macro-invertebrate decomposers (T.

ponticus, P. lamellatus, H. couchii, O. gammarellus,

O. mediterranea and T. deshayesii) and primary pro-

ducers (S. maritima-decomposing leaves, Sarcocornia

spp., Z. noltii-decomposing leaves, Bostrichia scor-

pioides, Enteromorpha spp. and A. portulacoides)

were collected from the salt marsh during the summer.

Animals were starved for 48 h to allow them to

evacuate food from their guts but as isopods take a

long time to empty their guts the isotope signal may

be influenced to a small extent by food still remaining

in the guts after these 2 days. The specimens were

killed by freezing and then washed with deionised

water, dried at 60 8C to constant mass and ground

to a fine powder. Samples for 13C were acidified with

10% HCl and then redried at 60 8C.Tissues of plant species were cleaned with deionised

water to remove all mud and detritus under a dissecting

microscope (magnification: 65 �). Samples were then

dried at 60 8C to constant mass. The dried tissues were

ground to a fine powder and samples for 13C were

checked under a dissecting microscope (magnification:

65�) for carbonate contamination using 10% HCl. For34S analysis ground plant tissue samples were re-sus-

pended in deionised water, centrifuged for 5 min and

the supernatant discarded. This procedure was repeated

twicemore and finally the sample was re-dried at 60 8C.Because of the low individual mass and to minimize

the variability associated with analysis of different

individual organisms a composite tissue sample from

more than one individual was used for all the species in

each isotope analysis (Carman and Fry, 2002; Vizzini

and Mazzola, 2002; Guest and Connolly, 2004).

Carbon and sulphur stable isotopes were analysed

at the Stable Isotope Laboratory, ICAT, Univ. of Lis-

bon. Carbon stable isotope analysis was done on a VG

ISOGAS SIRA II (Manchester UK) stable isotope

ratio mass spectrometer, working on continuous

flow mode coupled to a EuroVector EuroEA (Milan,

Italy) elemental analyser for sample automated prep-

aration. Internal Laboratory Standard UR=EA (cali-

brated against International IAEA (Vienna) standards

IAEA CH 6 and I=AEA CH 7) was used for calibra-

tion and replication assessment. The results were

expressed in the usual notation as a per mil (x)

deviation of the 13C/ 12C ratio in the sample from

the CDT (Canyon Diablo Triolite) standard. Average

precision for the batch run was 0.12x.

Sulphur stable isotope ratios were obtained through

extraction of total sulphur following the Eschka pro-

cedure (Chakrabarti, 1978). Sulphur was precipitated

as BaSO4 and analysed on a Micromass Isoprime

(Manchester, UK) stable isotope ratio mass spectrom-

eter, working on continuous flow mode coupled to an

EuroVector EuroEA elemental analyser for automated

sample processing. International IAEA (Vienna) stan-

dards IAEA S 1 and IAEA-NBS=123 were analysed

on the same batch runs as the samples for calibration

and replication assessment. The results were expressed

as a per mil (x) deviation of the 34S / 32S ratio in the

sample from the CDT (Canyon Diablo Triolite) stan-

dard. Average precision for the batch run was 0.3x.

2.4. Preference and feeding rate tests

Salt marsh peracarids live close to the upper marsh

where there are deposits of freshly detached and dead

leaves of plants from the salt marsh and the lagoon as

well as algae. Themost available potential food items in

the field were freshly detached but still green leaves of

Z. noltii, decomposing Z. noltii and decomposing S.

maritima, the green alga Enteromorpha spp. (fresh),

dead animals of the species to be tested. Food was col-

lected at the same site from which animals had been

sampled. The experiments were done in Petri dishes

(18.5 cm diameter�4 cm height) with a base of moist-

ened sand. In the case of T. ponticus plastic jars (10 cm


diameter�16 cm height) were used instead so that

specimens could burrow into the sand which was col-

lected at the sampling site and ashed for 3 h at 450 8Cprior to use, to make sure that the animals could not

feed on any microorganism or any other organic matter

attached to the substratum. Distilled water was added to

7F1% moisture in the substrate in order to simulate

natural sand moisture in the high marsh. In the case of

H. couchii and the amphipods, the containers were

covered with the respective Petri dishes lids, but for

T. ponticus and P. lamellatus containers were covered

with a 500 A mesh. Because the amphipods live sym-

patrically and were too active, it was not possible to

separate the species alive without harming them. There-

fore, groups of amphipods were used instead and the

different species were identified at the end of each

experiment when animals were killed. For the same

reason the lengths of all the animals were measured at

the end of the experiments. Experiments were run inside

a controlled environment cabinet with a temperature of

16F1 8C and a 12 :12 h light : dark cycle, which rep-

resent mean annual values for the field study sites.

For the preference tests, three replicates with thirty

animals in each were used. Experimental animals

were starved for 24 h prior to the multiple-choice

tests (Constantini and Rossi, 1995; Giannotti and

McGlathery, 2001; Silliman et al., 2004). Multiple-

choice assays were performed for 2 days by offering

equivalent masses of the different foods. Food items

were progressively removed when z50% was eaten

in order to determine the rank order of preference for

all the food types. In the isopod experiments, more

than 50% of the leaves of Zostera and Spartina were

rarely eaten at the end of the 2 days. The relative

ranking of these food types was therefore determined

by estimating the proportions of food offered that was

eaten. The group of amphipods in these experiments

was composed, on average, of 56% of O. mediterra-

nea and 44% of O. gammarellus.

For the palatability experiments nine replicates

with approximately thirty animals in each experiment

were run. Three other control boxes contained only

food without animals, to control for the autogeneous

change in the mass of each food type (always less than

5%). Animals were not starved for these experiments

to avoid hyperphagy when exposed to the test foods.

Test animals were given measured areas of Spartina

and Zostera or known wet masses of Enteromorpha at

the start of the experiment. Identical areas and wet

masses of test foods were dried (60 8C, 48 h) and

ashed (450 8C, 3 h) to estimate ash free dry mass

(AFDM) of foods offered. At the end of the experi-

ment the remains of foods were dried and ashed so

that consumption rates expressed as AFDM could be

determined. The mass losses were corrected for au-

togenous loses from identical sized samples which

had not been exposed to the animals. Consumption

rates were measured within variable periods (1 to 20

days) according to the grazing rate of each species

which also varied according to the type of food.

Periods as long as 20 days were necessary because

isopods ate negligible amounts of Zostera and Spar-

tina. The average composition of the amphipod group

for these experiments was: Enteromorpha (54% O.

gammarellus, 45% O. mediterranea, 1% T. deshaye-

sii), animal matter (66% O. gammarellus, 34% O.

mediterranea), Spartina (66% O. gammarellus, 34%

O. mediterranea), green Zostera (55% O. gammar-

ellus, 45% O. mediterranea), decomposing Zostera

(23% O. gammarellus, 76% O. mediterranea).

2.5. Relative growth rates

Relative growth rates for each of the species in the

salt marsh were obtained from size-frequency analysis

of the lengths of individuals (Sunderland et al., 1976;

Hassall and Dangerfield, 1990, 1997) extracted from

cores and pitfall traps taken randomly from between

neap and spring high tide levels on the upper salt

marsh shore during 1998 and 1999 as described by

Dias and Hassall (in press-a). Cohort growth curves

were constructed and the size of females in their first

breeding season was used as size at time t, in con-

junction with the size of newly released offspring for

size at time t0, as described in detail by Dias (2003)

and Dias and Hassall (in press-a) to calculate relative

growth rates as defined by van Emden (1969).

3. Results

3.1. Qualitative differences in diet

3.1.1. Gut content analysis

On average 72.5% of the hindgut contents of

these macro-decomposers was identifiable. Zostera

Table 2

Percentage of the contents in the guts of isopods and amphipods inhabiting the upper marsh

Zostera Spartina Green algae Undetermined vegetal detritus Diatoms

T. ponticus 55.9F4.8a – 8.1F2.5a 35.9F4.5 –

P. lamellatus 60.7F5.3a,b – 0.16F0.1b 33.8F5.3 –

H. couchii 85.9F3.2c – 0.2F0.1b 13.8F3.2 –

O. gammarellus 76.5F4b,c 8.4F2.3 – 15.1F4.0 +

O. mediterranea 64.7F5.4a,b – 0.2F0.2b 35.1F5.4 –

T. deshayesii 68.7F5.3a,b,c – – 31.3F5.3 –

MeanFSE, n =50. Significance of difference between the several consumers for each gut content: 1-way ANOVA, Zostera ( F =5.2,

P b0.0001), green algae ( F =9.9, P b0.0001). Mean values within a food category with different letters differ at P b0.05 (Tuckey test).


has very distinctive epidermal cells so the proportions

of this item in the gut contents could be identified

quite reliably. The two species with the highest pro-

portions of Zostera in their gut contents were H.

couchii, an isopod, and O. gammarellus, an amphi-

pod (Table 2). Zostera comprised over 50% of the

gut contents for all the species but comprised signif-

icantly less of the gut contents of T. ponticus than for

either O. gammarellus or H. couchii. There were no

significant differences between the other two isopods

and the other two amphipods in this respect. Only

one of the amphipods (O. mediterranea), but all three

isopods, had green algae in their hindguts but, except

for T. ponticus, it was only present in very small

amounts of less than 1% of the gut contents. These

results do not, therefore, provide any clear cut evi-

B

SaH

P

A

Sp

Ty

Z

E

OgOm

Ta

6

8

10

12

14

16

18

20

-35 -30 -25 -20 -15 -10 -5

δ34S

(‰

)de

plet

eden

riche

d

δ13C (‰)depleted enriched

Fig. 1. Stable carbon and sulphur isotope ratios (meanFSD) of salt

marsh producers: Atriplex portulacoides (A), Bostrichia scorpioides

(B), Enteromorpha spp. (E), Sarcocornia spp. (Sa), Spartina mar-

itima (decomposing leaves) (Sp), Zostera noltii (decomposing

leaves) (Z); and consumers: Halophiloscia couchii (H), Orchestia

gammarellus (Og), Orchestia mediterranea (Om), Porcellio lamel-

latus (P), Talorchestia deshayesii (Ta) and Tylos ponticus (Ty).

dence of resource partitioning between the two orders

of peracarids examined.

3.1.2. Stable isotope analysis

Results of the stable isotope analysis (Fig. 1,

Table 3) confirm the pattern already observed

from the results of the gut contents analyses: that

there are no consistent differences between amphi-

pods and isopods in the isotopic consequences of

their feeding. The isopod H. couchii occupied an

intermediate position between the two amphipods O.

mediterranea and T. deshayesii in respect of their

sulphur signals suggesting that it had fed on a

combination of foods with a very similar range of

isotopic sulphur signals. Similarly, all the isopods

and the amphipod O. gammarellus lie in an inter-

Table 3

Stable isotope ratios (x) of consumers and primary producers

(vascular salt marsh plants, seagrasses and macroalgae) collected

from a Ria Formosa lagoon salt marsh

Material d13C d34S

Consumers

Tylos ponticus �21.0F0.2 8.7F0.1

Porcellio lamellatus �21.7F0.1 13.3F0.02

Halophiloscia couchii �23.8F0.2 14.1F0.2

Orchestia gammarellus �19.1F0.1 14.3F0.04

Orchestia mediterranea �24.9F0.2 14.8F0.5

Talorchestia deshayesii �25.6F0.1 13.9F0.1

Vascular salt marsh plants

Spartina maritima �14.5F0.1 12.0F0.3

Atriplex portulacoides �21.1F0.1 14.8F0.1

Sarcocornia spp. �26.2F0.1 15.6F0.04

Seagrasses

Zostera noltii �11.2F0.2 17.2F0.02

Macroalgae

Entermorpha spp. �16.4F0.1 19.5F0.2

Bostrichia scorpioides �30.6F0.03 16.8F0.03

Data are mean y valuesFSD, n =3.

Table 4

Food preferences of isopods and amphipods for foods from the Ria Formosa salt marsh

Animal matter Enteromorpha Spartina Fresh Zostera Decomposing Zostera

H. couchii 5 4 3 1.5 1.5

P. lamellatus 5 4 3 1.5 1.5

T. ponticus 5 4 3 1.5 1.5

Amphipods 4 5 2.5 2.5 1

Scores are given as mean ranks where a low number indicates a lower preference for a food and high numbers a high preference, n =30.

Significance of differences between food items: Krustal-Wallis, H. couchii (H =12.1, P b0.02), P. lamellatus (H =11.2, P b0.02), T. ponticus

(H =12.1, P b0.02), amphipods (H =12.1, P b0.02).


mediate position between these two amphipods with

respect to the carbon signal. These results suggest

that there is no clear distinction between members

of the two orders in respect to the isotopic signals

Enteromorphac

ac

bab

0

0.5

1

1.5

2

2.5

3

H. couchii P. lamellatus T. ponticus Amphipods



RC

R (

log

mg

g-1 d

ay-1

)R

CR

(lo

g m

g g-1

day

-1)

-1-1

-1-1

RC

R (

log

mg

g-1 d

ay-1

)

Decomposing Zosterab

aaa

0

0.2

0.4

0.6

0.8

1

Animal matter

b

aa

a

0

0.5

1

1.5

2

2.5

Fig. 2. Feeding rates (RCR) (meanFSE) (log mg g�1 day�1) on the test fo

lamellatus, Tylos ponticus and the amphipods. Significance of difference

omorpha ( F =10.6, P b0.001), Spartina ( F =14.0, P b0.001), decomposin

animal matter ( F =21.1, P b0.001). Different letter above bars indicate si

of the foods they fed upon in the field prior to these

analyses and that there is no clear niche differenti-

ation between them in qualitative aspects of their

trophic interactions.



RC

R (

log

mg

g d

ay)

RC

R (

log

mg

g d

ay)

Spartina

b

c

ab

ac

0

0.2

0.4

0.6

0.8

1

1.2

1.4

Green Zostera

b

aa

a

0

0.2

0.4

0.6

0.8

1

1.2

ods for each salt marsh consumer: Halophiloscia couchii, Porcellio

s between consumers for each food item: 1-way ANOVA, Enter-

g Zostera ( F =82.7, P b0.001), green Zostera ( F =27.3, P b0.001),

gnificant difference among species (Tukey test, P b0.05).

Table 5

Mean (F1 SE) relative consumption rates (RCR) (mg g�1 day�1), n =30

T. ponticus P. lamellatus H. couchii Amphipods A/ I

Enteromorpha 183.2 (20.8) 132.4 (88.6) 124.6 (45.3) 424.4 (49.4) 3.2

Animal matter 10.4 (0.07) 28.3 (10.5) 56.8 (11.2) 135.5 (18.0) 4.3

Spartina 0.2 (0.1) 0.0028 (0.87) 7.1 (2.0) 19.7 (6.0) 8.2

Green Zostera 0.04 (0.01) 0.1 (0.04) 0.6 (0.2) 8.8 (2.9) 35.2

Decomposing Zostera 0.005 (0.001) 0.1 (0.07) 0.2 (0.08) 7.3 (1.5) 73

The right column shows the ratio of the mean values for consumption rates of amphipods (A) to average consumption rates for the three species

of isopods (I).


3.1.3. Food preference tests

In the laboratory when offered unrestricted access

to a range of food items, chosen on the basis of their

known potential availability in the field, all the test

groups showed similar preferences. The order of

preference between the isopod species was very

consistent, with the most preferred food being dead

animals, followed by Enteromorpha, and Spartina

with freshly dead and decayed Zostera being the

least preferred (Table 4). When given an opportunity

all the isopods prefer to scavenge from dead con-

specifics and their next most preferred food were

green algae, then Spartina. For the amphipods the

order of preference was similar to that of the iso-

pods, the difference being that the first choice was

for green algae, and dead conspecifics were their

second most preferred food followed by Spartina

Fig. 3. Relative growth rates (RGR) (meanFSE) of salt marsh consume

ponticus) and amphipods (Orchestia mediterranea, Orchestia gammarel

( F =70049, P b0.001) followed by Tukey test for multiple comparisons

species ( P b0.05).

and fresh Zostera with decomposing leaves of Zos-

tera being least preferred (Table 4).

3.2. Quantitative differences in feeding rates

The rates at which the isopods and amphipods

consumed each of the potential diet items offered

alone, are shown in Fig. 2. This shows that for most

of the different foods the amphipods ate significantly

more than any of the isopods, except for Enteromor-

pha where there were no significance differences

between amphipods and T. ponticus and for Spartina

where there were no significant differences between

amphipods and H. couchii. The ratios of mean values

for the consumption rates of the three species of

isopod are compared with those of the amphipods

fed on the same foods in the same arenas under the

rs: isopods (Halophiloscia couchii, Porcellio lamellatus and Tylos

lus and Talorchestia deshayesii). Analyses are by 1-way ANOVA

: different letters above bars indicate significant difference among


same microclimatic conditions in Table 5. For all of

the potential food items used, the amphipods fed a lot

faster than the isopods (3 to 1460�).

The only food for which there were any significant

differences between the different isopods was for

Enteromorpha which T. ponticus ate significantly

faster than did the other two species. This is consistent

with the results of the gut contents analyses which

showed that T. ponticus had significantly more of this

food in its hindgut than either of the other two isopods

(t=31, P b0.0005).

3.3. Relative growth rates

The rates at which each species grows in the field

were compared as relative growth rates in Fig. 3.

There is a striking parallel between differences in

consumption rates and differences in growth rates

between members of the two orders, in that all three

of the amphipods have significantly higher relative

growth rates than any of the isopod species (Fig. 3).

4. Discussion

All three of the different methods of diet analysis

showed that these amphipods and isopods have broad

and overlapping diets. The analyses of hindgut con-

tents are limited to food parts that have not been

digested. If the two orders have different digestive

efficiencies, this could affect the comparison between

them. Terrestrial isopods have a typholosole in the

dorsal wall of the anterior hindgut which enable them

to increase their digestive efficiency by using it as

functional midgut (Hassall and Jennings, 1975;

Hames and Hopkin, 1989). In contrast, a typholosole

is not mentioned as being part the digestive anatomy

of amphipods described by Schmitz (1967) or Martin

(1964). It might be predicted therefore that the less

efficient amphipods would retain more of the easily

digested foods than isopods. However, it was the

isopod T. ponticus that had significantly more of the

digestible algae than any of the other species, suggest-

ing that comparisons between the groups are not

invalidated by any differences in digestive efficiency

there may be between them.

Higher plant tissues persist for much longer than

algae in the gut contents but can only be identified

when particular distinctive cell patterns are visible.

The epidermis of Zostera was particularly distinctive

but there is no reason why it should be more dis-

tinctive in the guts of any one species. Therefore,

comparisons of proportions of Zostera in the diet of

the different species do give an indication of the

relative extent to which they utilize it in the field.

The species that had both the highest and the lowest

proportion of Zostera in the gut contents were both

isopods, while the three amphipods and the other

isopod had intermediate amounts. This indicates

that there is no simple division between members

of the different orders in the extent to which they

utilize this very common potential food resource in

the field.

A more long-term integration of the trophic his-

tory of an animal can be obtained from stable iso-

tope analyses. The results of comparing the carbon

and sulphur isotope ratios for the six test species

again showed no clear distinction between the

amphipods and isopods. The carbon isotope ratios

for all the isopods lie between those of the different

amphipod species. The sulphur isotope ratios for all,

except one of the study species, are also very sim-

ilar, the exception being T. ponticus which has a

very depleted signal much closer to that for partic-

ular organic matter (Machas and Santos, 1999) than

for any of the other species or for other potential

foods that were analyzed. This may reflect an im-

portant difference in its dietary history in the field

especially as it had significantly more algae, and

significantly less Zostera in its gut contents, than

some of the other species.

When offered only one species of potential food at

a time, there were no significant differences between

the different species of isopods but there was a very

significant difference between the three isopods and

the amphipods for each of the food items. In multiple-

choice experiments in the laboratory, for both isopods

and amphipods, Zostera was clearly the least pre-

ferred of the foods offered whether in relatively

fresh or decomposing condition. Litter from the

other higher plant, Spartina, was preferred to Zostera

but for both amphipods and isopods the two most

digestible food items: green algae and other animal

tissues were the most preferred. Potentially their high

digestibility could account for the differences between

results of the food preference tests and the gut con-


tents analyses. However, no fragments of cuticle were

observed during analyses of the gut contents of over

350 specimens from the field.

Thus, the first hypothesis that the greater success of

amphipods in salt marshes results from them exploit-

ing a qualitatively different diet to the isopods is not

supported by any of the laboratory observations. This

suggests that there are no differences in either funda-

mental niche (food preferences) or realised niche (gut

contents and stable isotope analyses) in relation to the

composition of their diets.

When offered only one food the amphipods ate

faster than the isopods (Table 5). The biggest differ-

ence (37–1460�) being for the decomposing Zostera

then green Zostera (35�), Spartina (8�), animal

matter (4�) and Enteromorpha (3�). This constitu-

tes a substantial qualitative difference in the way in

which amphipods and isopods in this salt marsh

process the available foods. There are some possible

mechanistic explanations for this. Amphipods are

shredders (Rong et al., 1995; Graca et al., 2001) in

the way in which they prepare foods for ingestion

using gnathopods to tear pieces of plant tissues. In

contrast, these terrestrial isopods do not have gnatho-

pods, the most posterior of their limbs that function

as mouthparts are their maxillipeds which although

bearing strong setae, do not have chelae as do the

gnathopods of amphipods and so cannot shred food

as efficiently or as fast. Internally, the hindgut of

amphipods is simpler than that of isopods in that it

lacks a typholosole which enables terrestrial isopods

to digest their food more thoroughly in the hindgut

(Hames and Hopkin, 1989).

Possibly, a consequence of these differences in

their ingestion and digestive strategies is that the

amphipods had a much higher growth rate than the

isopods (Fig. 3). They could therefore reach repro-

ductive size earlier with shorter generation times.

None of these species of isopod mature in less than

10 months compared, with 4 months for some of the

amphipods, which have a continuous rather than sea-

sonal breeding phenology (Dias and Hassall, in press-

a). Also, as fecundity is size-related, they may also

have larger broods than the isopods (Dias and Hassall,

in press-a).

If they had similar pre-reproductive mortality rates

the suite of life-history traits that results from their

rapid resource processing strategies, would give

amphipods the potential for a higher rate of natural

increase than is the case for the isopods. The latter, are

constrained by resource acquisition strategies evolved

to enable them to survive severe temporal heteroge-

neity in suitability of foraging conditions such as

prolonged and unpredictable periods of drought in

the drier terrestrial environment. These resource pro-

cessing strategies are likely to lead to slower growth

rates, longer development times and longer generation

times. Thus, lower intrinsic rates of population in-

crease than the amphipods could help to explain

why they are often less successful in exploiting salt

marsh habitats. The reasons why T. ponticus appears

to be an exception to this generalization are explored

by Dias and Hassall (in press-b).

Acknowledgments

The authors acknowledge the late Dr. M. Sprung

for his help and guidance in designing the project. Dr.

Cristina Maguas and Dr. Rodrigo Maia from the

Stable Isotope Laboratory, ICAT, University of Lis-

bon, for performing carbon and sulphur stable isotope

analyses. The first author acknowledges financial sup-

port by the Fundacao para a Ciencia e Tecnologia

(grant PRAXIS XXI/BD/11039/97). [RH]

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Food, feeding and growth rates of peracarid macro-decomposers in a Ria Formosa salt marsh, southern Portugal