We analyze fue dynamics of fue gastropod cornmunity living in fue Ebro Delta ricefields in relation to fue cultivation cycle. We found six bassornmatophoran ...
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Hydrobiologia 337: 85-92, 1996.
@ 1996Kluwer AcademicPublishers. Printed in Belgium.
Succession and secondary production of gastropods in the Ebro Delta ricefields JacobGonzález-Solís & XavierRuiz fl
Dept. Biologia Animal (Vertebrats), Facultat de Biologia de la Universitat de Barcelona, Av. Diagonal 645, Barcelona 08028, Spain
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Received 12July 1995;in revisedfonn 21May 1996;accepted 4 June1996
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Key words: agroecosystem, breeding cycles, pulmonates, availability
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Abstract We analyze fue dynamics of fue gastropod cornmunity living in fue Ebro Delta ricefields in relation to fue cultivation cycle. We found six bassornmatophoran species, three of which form more than 97% of total: Physella acuta (Draparnaud), Planorbis planorbis (L.), and Lymnaea avara (L.). Colonization of ricefields by freshwater pulmonates started in June, with populations increasing until fue harvest in October, when fue bulk of gastropods showed a decline. Populations recovered quickly and, in some cases reached their yearly maximum of abundance in Autumn. P. acuta predominates ayer all other species except in May and June, when P. planorbis takes overoL. avara is always fue least abundant of fue three main species. The analysis of size classessuggeststhat fueTeare two breeding seasonsfor P. acuta and P.planorbis, fue first at fue end of Surnmer, with a total replacement afilie population, and fue second in October-November, without replacement. Conversely, L. avara shows a wide array of size classesthroughout fue rice cultivation cycle. This suggeststhat this species breeds earlier and outside fue ricefields. The variations in population numbers of each species in relation to environmental changes induced by rice cultivation suggest that P. planorbis better exploits fue algal cover or other food available at fue ricefield bottoms, while P. acuta forages mainly on epiphytic vegetation and adventitious plants. Gastropod secondary production and turnover ratios in fue Ebro Delta fall within fue range of natural freshwater systems, but are situated in fue zone of higher values.
r'" Introduction
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Freshwater gastropods make up a large proportion of benthic animal biomass in variable aquatic habitats
(McMahon, 1983;Bosniaet al., 1990).This is because semelparity,shortlife spans,earlyageat maturity,high growth rates, and high reproductivecapacitiesmaximize fue production of offspring in variableenvironments (McMahon, 1983).They may therebyprovide an important sourceof food for a variety of predators (Bosniaet al., 1990;Crowl & Covich, 1990;Wollheim & Lovvom, 1995). Moreover, their role in aquatic ecosystemsseemscrucial to fue growth and mainteDanceof macrophytes(Underwood& Thomas,1990; Underwood,1991).
Ricefields are extreme examples of variable aquatic habitats, owing to pesticide treatrnents, adjustrnents in water level and other agricultural operations (Forés & Comín, 1986). Freshwater gastropod communities
may playa keystonerole in fue transferof matterand energy in fuese agroecosystems.Also ricefields are often situatedin ancientwetlandareasof alluvial plains or deltas, where they benefit from periodic natural flooding (Forés& Comín, 1992).By the progressive loss of wetland habitatsin Europeduring the present century(Finlaysonet al., 1992),ricefieldsare now fue only majar flooded areasavailablefor invertebrates, fish, andwaterbirds(Fasola& Ruiz, 1996). Ricefieldsprovideexcellentlarge-scaleexperimental field situations,which can be usedto comparefue ecology of their communitieswith those of perma-
86 nent and/or less variable habitats (Brown, 1991). Yet fue biology and dynamics of gastropod communities in such habitats is poorly known (but seeKurihara, 1989). Among the ecological parameters characterizing fue population dynamics of freshwater gastropods there is production ecology, which quantifies their ecological strategies in different types of aquatic ecosystems (Russell-Hunter & Buckley, 1983). As part of a larger study on fue role of ricefields in fue ecology of waterbirds in the Ebro Delta, fue gastropod community of fue Ebro Delta ricefields is here described, and related to natural and human induced changes in that agroecosystem. Gastropod secondary production is also estimated, and compared to that in other ecosystems.
focussed on potential prey for waterbirds. This underestimates fue smaller-sized gastropods, but only a negligible deviation in production values, since fue production by fuese size classes is small. Organisms were immediately frozen for analysis. A range of eight to 12 monthly samples were taken. We took at least one sample from each of fue five ricefields, and replicated when possible (Table 1). Sampling points were randomly selected between one and tour meters from fue shore. Sampled ricefields were selected to account for differences in timing of agricultural operations, which create a patchy rather than homogeneous environment in the Ebro Delta (González-Solís et al., 1996). Analysis ~
Material & methods Studyarea The study was performed in the ricefields of fue southern half of fue Ebro Delta (40 °42'N, O °51'E). Here ricefields occupy about 15000 ha (Ferrer & Martinez, 1987) and communicate by a web ofirrigation and drainage canals which flow into littoral lagoons surrounding fue afea. In fue Mediterranean region, rice needs 130-180 days to mature. Agricultural operations include land preparation and fertilization (March), flooding and sowing (April), germination, growth and application of algicides and herbicides (May-June) and of insecticides (July-August). The flowering (July), maturation (August-September) and harvesting (September-October) of rice, complete fue cycle of cultivation (Figure 1). The water flow to ricefields stops once fue rice is harvested and fue stubble is burnt and buried. However, some fields are maintained well flooded after harvesting for hunting purposes. A summary of fue limnological characteristics of fue Ebro Delta ricefields is given in Forés & Comín (1992). Sampling Five ricefields were sampled from May to December 1991, during fue first week of each month. Samples were obtained by sinking a metallic square of 60 cm sirle and 40 cm in height down to 5 cm in fue muddy soil. The contents were filtered through a sieve of 1.8 mm mesh, to separate organisms from soil and water. This sieve was used becauseour studies mainly
All gastropods of about 2 mm in length or larger were selected, identified, counted and measured :i: 0.1 mm) using a micrometer installed on a binocular lens (1040 x). A sub-sample of individuals of different sizes of each of fue three main species (Physella acuta (Draparnaud), Planorbis planorbis(L.) andLymnaea ovata (L.)) was selected to define fue relationship between shelllength and snail dry weight. Water content was determined by drying snails in an oyen at 60 °C to constant weight. For linear relationship between biomass and length, data were log transformed. Energy values were calculated from standard values for lipid and lean dry mass fractions (largely protein, therefore applying protein value to such fraction). Lipid contents were determined only for P. acuta, using a sub-sample of five collections, each collection containing 66 individuals, extracted in a soxhlet apparatus with n-hexane as a solvento Secondary productivity was estimated using fue size frequency method (c.f. Hynes & Coleman, 1968), and modifications of this method by Hamilton (1969), and Benke (1979). Since samples from different ricefields might combine different cohorts, our estimates correspond to global values for each species and were performed considering only those months in which we detected gastropods (May to December). We also assumedthat CPI (cohort production interval) is 1 year. Individual dry weight biomass values were derived fromregressionequationandmeanvaluesforeachsize class obtained by averaging fue individual estimates.
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87
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Figure l. Diagrarn
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of rice cultivation
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A'
A
My. . In.H . I Iu.'
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cycle in the Ebro Delta. The an-ows indicate the different
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pesticide treatrnents:
D
.N°
A
=aIguicides. H = herbicides.
and i = insecticides. Table l. Monthly average density (individuaIs measuring 2 mm or larger per m2) of the different gastropod species found in the Ebro Delta ricefields. N
May Jun Jul Aug Set Oct Nov Dec
8 10 12 10 11 11 10 12
P. planorbis
L. avara
x
P. acuta
sd
x
x
0.35 14.17 197.45 263.61 245.45 99.75 563.61 411.57
0.98 23.95 158.48 179.71 350.01 135.76 452.06 503.21
14.24 34.87 40.00 56.84 49.77 43.27 69.72 93.41 49.24 79.14 58.08 117.87 270.28 445.32 97.45 96.43
Total 84 232.41 333.21
f'
,
sd
81.68 179.33
sd
L truncatula
Succinea sp.
B. tentaculata
x
x
x
sd
0.69 0.00 0.00 0.00 0.00 0.51 0.00 1.62
1.96 0.00 0.00 0.00 0.00 1.12 0.00 4.01
sd
sd
0.00 0.00 0.28 0.88 33.80 62.42 72.22 141.97 39.90 74.02 17.42 26.38 1.11 2.68 5.79 8.33
1.74 4.91 1.11 2.68 0.23 0.80 0.28 0.88 0.00 0.00 1.52 5.03 0.83 1.87 8.56 22.98
0.35 0.98 0.00 0.00 2.31 3.71 2.78 3.93 1.77 2.85 1.52 2.28 11.94 18.57 1.39 2.78
63.40
1.88 9.18
2.74 7.47
21.92
0.36 1.71
Results
showed similar and low biomass from May to October
Six speciesof gastropods live in fueEbroDeltarice-
and peaked in November. though at values much lower thanthosereached by 1':acuta.
fields: 1': acuta, 1':planorbis, L. ovata, L. truncatula (Müller), Succinea,Draparnaud,sp. and Bithynia tentaculata (L.). Table 1 gives data on averagedensity per m2for thesespecies,of fuesefue former threerepresentan averageof 97% of all gastropodscollected (n = 10,403).All resultsand discussionhereafterwill refer to only fuesethree species.Monthly total biomassvariation of 1': acuta, 1':planorbis and L. ovata is given in Figure 2. 1': acuta is fue specieswith fue higher biomassvalues,with two noticeablepeaks,in July andin December.In AugustL. ovatapeaked,and was double the value of 1': acuta, while in September both specieshad a similar biomass.1':planorbis
Thecomparisonofbiomasswith density(individuals m-2) (Table1) showsthat 1':planorbis hadhighest averagedensity in May and June. although fue biomassof 1': acuta in June was much higher than that of 1':planorbis, indicatingthat adult forms of P. acuta were colonizing fue ricefield. 1': acuta showedhigher density valuesthan any other speciesfrom July to December,and peakedin August and November.In August fue biomassof 1': acuta was lower than in July, indicating fue appearanceof smaller, juvenile forms.Thesejuvenile forms decreased in numberuntil November.but averagebiomassvaluesin the ricefield were maintained,indicating growth. Theseindividu-
88 Table 2. Annual productivity of Phy.~e[[aacuta, Lymnaea avara and Planarbis planarbis in fue Ebro Delta ricefields. = grams of dry weight biomass of fue size interval per m2, W = weight at loss, PSI = production per size interval (W x bo N x Number of Intervals). Note fue lack of data corresponding to size interval between 0-0.9 mm, and that figures corresponding to the first size intervals are negative, owing to underestimation. These values have been omitted in
A.d.w. = Average dry weight ofthe size interval, N = number ofindividuals ofthe size interval per m2, B
the surnrnatory term of productivity by size intervalo
SizeInterval
A.d.w. (g)
N (ind.m2).
B (d.w. g m2)
1-1.9 rnrn 2-2.9 rnrn
2.5 x 10-5 7.9 x lOS
1 x 10-5 3.6 x 10-3
3-3.9rnrn
2.12x 10-4
4-4.9 rnrn 5-5.9 rnrn 6-6.9 rnrn
4.89 x 10-4 9.74 x 10-4 1.672 x 10-3
1.71 45.93 67.82 60.83 55.69 47.31
2.89 x 10-2 5.43 x 10-2 7.91 x 10-2
10-3 10-3 10-3 10-3 10-2 10-2
28.61 9.95 1.71 0.74 0.09 0.05
7.61 x 4.02 x 1.02 x 6.2 x 1.2 x 7x
A.d.w. (g)
N (ind.m2).
7-7.9 rnrn 8-8.9 rnrn 9-9.9 rnrn 10-10.9 rnrn 11-11.9 rnrn 12-12.9 mm SizeInterval 1-1.9 mm 2-2.9 rnrn 3-3.9 rnrn 4-4.9 rnrn 5-5.9 rnrn 6-6.9 rnrn 7-7.9 rnrn 8-8.9 rnrn 9-9.9 rnrn 10-10.9rnrn 11-11.9 rnrn Size Interval
2.659 x 4.035 x 5.968 x 8.365 x 1.2807x 1.5372x
2.5 x 8.1 x 2.37 x 5.32 x 1.057 x 1.864 x 2.885 x 4.744 x 6.873 x 9.261 x 1.2725x
10-5 10-5 10-4 10-4 10-3 10-3 10-3 10-3 10-3 10-3 10-2
A.d.w. (g)
1.43x 10-2
B (d.w. g m2)
0.14 1.90 4.68 7.36 7.59 4.58 2.64 1.25 0.37 0.14 0.05 N (ind.m2).
10-2 10-2 10-2 10-3 10-3 10-4
1.0 x 2.0 x 1.1 x 3.9 x 8.0 x 8.5 x 7.6 x 5.9 x 2.5 x 1.3 x 6.0 x
10-5 10-5 10-3 10-3 10-3 10-3 10-3 10-3 10-3 10-3 10-4
B (d.w. g m2)
-44.21 -21.90 6.99 5.14 8.38 18.70 18.66 8.24 0.97 0.65 0.05 0.05
-1.76 2.78 2.69 -0.23 3.01 1.94 1.39 0.88 0.23 0.09 0.05
5.2 x 10-5 1.45 x 10-4
-0.02996 -0.04140
3.50x 10-4 7.32 x 10-4 1.323x 10-3 2.166 x 10-3 3.347 x 5.001 x 7.166 x 1.0586x 1.4090x 1.5372x
5.3 x 1.59 x 3.85 x 7.94 x 1.461 x 2.375 x 3.814 x 5.808 x 8.067 x 1.0993x 1.2725x
10-4 10-4 10-4 10-4
0.88 9.35 32.50 33.80
2.0 x 2.4 x 1.18 x 1.65 x
10-4 10-3 10-2 10-2
-8.47 -23.15 -1.30 14.54
6-6.9 rnrn 7-7.9 rnrn
6.33 x 7.99 x 9.69 x 1.113 x
10-4 10-4
19.26 10.74
1.22 x 10-2 8.6 x 10-3
10-4
6.30
10-3
1.20
2.14 x 3.10 x 4.27 x 5.61 x
0.03185 0.04889 0.14414 0.52657
10-3 10-3 10-3 10-2 10-2 10-2
0.81180 0.53578 0.09057 0.08919 0.00848 0.00925
W
PSI (g m2)
10-5 10-4 10-4 10-4 10-3 10-3 10-3 10-3 10-3 10-2 10-2
-0.00112 -0.00531 -0.01239 -0.00221 0.05275 0.05540 0.06357 0.06131 0.02241 0.01221 0.00707
W
boN
1.72 x 2.57 x 3.64 x 4.89 x
8-8.9rnrn
PSI (g m2)
boN
2-2.9 rnrn 3-3.9 rnrn 4-4.9rnrn 5-5.9 rnrn
9-9.9 rnrn
W
boN
'
~
PSI (g m2)
10-4 10-4 10-4 10-4
-0.01816 0.07180 -0.00553 0.08158
8.52 4.44
7.16 x 10-4 8.84 x 10-4
0.06099 0.03930
6.1 x 10-3
5.09
1.505x 10-3
0.05349
1.4 x 10-3
1.20
1.131x 10-3
0.01361
als reachedmaturity in November,when fue density
ing fue appearance of juveniles. In L. ovata valuesof
peakedagain, while maximum biomasswas recorded in December,despitedepletion of density, again indicating growth. P. planorbis and L. ovata presentedparallel variation of biomassand density, though for fue former, fue densitypeakin Novemberwasfive fold fue values of October,whereasbiomassvaluesdoubled.indicat-
densityandbiomassvariedin parallel. For P.acutaandP.planorbisfue smallestsizeclasseswerefound from Augustto SeptemberandNovember to December,while fue largestdisappearedin July andemergedin December(Figure3). In L. ovataricefields werecolonizedsimultaneouslyby individualsof all size classes(Figure 3c). Theseindividuals disap-
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89 Phyeell.
E
.cuta
1
~ 0,8 ...
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.c 0,8 ...
f
0,4
...
~
~ 0,2
9 mm size intervals, and is about one arder of magni...
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c
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ec
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Lymn... Oy.ta
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In L. avara,suchdifferencescanbe attributedto lower density.In contrast,fue densityof P.planorbis is half that of P. acuta, but its biomasswas much lower than in fue other two species.P. acuta productivity values Turnover(P/B), however,is more similarforallthe
0,8
::: .c
tudehigherthanthatoftheothertwo species(Table2).
were much larger than fue other two species (Table 3).
1
N
marinesnail tissue,to obtain 538.53mgC g-1 of gastropod(d.w.).Weassumedthesamepercentageoflipid contentsfor L. avaraandP.planorbis in arderto obtain estimatesfor fuesetwo species. P.acutaannualproductivity peakedbetween6 and
three species. 0,8
~
0,4
~
r--
.0;
O 0,2 a
...
. . .
O M.y.lu
. . . . . . u
ug
PI.norble
et
.
Oct
. . Noy
. .
. .
Oec
~ 0,8
thefirstattheendofSummer,withatotalreplacementofthepopulation, and the second in Autumn
~O,8
~ 0.4
g a
-......
0,2
..............
(October-November), without replacement, i.e., a univoltine pattern type C (Calow, 1978), but with repro-
O M.y
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.lul
Aug
aet
Oct
Noy
Oec
Figure2. Monthlyvariationof meanbiomass (grarnsof dryweight m-2) for the threegastropod speciesmoreabundant in theEbro Deltaricefields.Barscorrespond to standard error.
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,
.
Life-cyclesofthe main species Plots of size classes(Figure 3) suggestthat there are two breedingseasonsfor P. acuta and P. planorbis, since there are two peaks of appearanceof smaller individuals(sizeclassesaround2 mm in shelllength),
pl.norble
1
E
N
DISCUSSIOn ' ,
pearedin Autumn, and somejuveniles reappearedin December,indicating that L. avarabreedsbeforecolonizing the ricefields,thoughtherewas a shortreproductiveperiod insidethe ricefield in December. The relationships between shell-length (in mm1.10-1) and dry weight biomass(in grams) for fue threemain speciesare significant: P. acuta, ,2 = 0.93, N=50, P< 0.0001; L. avara, ,2=0.80, N=85, P
