Types of response to environmental changes in cladoceran populations

Bolletino di zoologia ISSN: 373-437 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/tizo9 Types of response to environmental changes in cladoceran populations Carla Bonacina, Riccardo de Bernardi & Maria Illuminata Taticchi To cite this article: Carla Bonacina, Riccardo de Bernardi & Maria Illuminata Taticchi (994) Types of response to environmental changes in cladoceran populations, Bolletino di zoologia, 6:4, 385-393, DOI:.8/259493559 To link to this article: http://dx.doi.org/.8/259493559 Published online: 28 Jan 29. Submit your article to this journal Article views: 77 View related articles Citing articles: 2 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalinformation?journalcode=tizo2 Download by: [48.25.235.26] Date: 8 February 26, At: 7:56

Boll. Zool. 6: 385-393 (994) Downloaded by [48.25.235.26] at 7:56 8 February 26 Types of response to environmental changes in cladoceran populations CARLA BONACINA RICCARDO DE BERNARDI C.N.R. Istituto Italiano di Idrobiologia, Pallanza (Italy) MARIA ILLUMINATA TATICCHI Istituto di Idrobiologia e Pescicoltura, Università di Perugia, via Elce di Sotto, I-63 Perugia (Italy) ABSTRACT Cladocerans are a usual component of lacustrine plankton, even though they are often characterized by low species numbers and high structural monotony. In most cases, population dynamics of cladoceran communities seems to be influenced by biotic interactions rather than by chemical and physical variations in the environment, if these occur in a nontraumatic way, because of the central role cladocerans play in the lacustrine food-chain and the relatively uniform tolerance displayed by different taxonomical entities towards the abiotic components of the system. In this paper we shall consider three situations that can be regarded as paradigmatic to illustrate different responses of cladoceran populations: the case of a great lake where environmental changes have occurred gradually over a long period of time (Lago Maggiore), that of a lake traumatically exposed to a massive toxic input and now in a phase of recovery (Lago d'orta), and lastly that of a shallow lake subject to sudden, severe changes in factors controlling water productivity (Lago Trasimeno). INTRODUCTION Cladocera are very suitable as material for studying the influence of environmental changes on animal communities, owing to their short life-span (about 3-5 days) and early maturation (about one week). In these respects, Cladocera differ greatly from Copepoda, which have a longer life-span (some months) and spend a much longer part of their life in the immature, pre-reproductive stages (according to Wutrich, 948, the mean duration of naupliar stages for a female diaptomid is about days), and from Rotifera which have a very short life and are often only present in the plankton community of lakes for a very brief period of time. Furthermore, it is relatively easy to satnple and determine cladocerans; finally, cladocerans are a very widespread group, and this makes it possible to compare community reactions in various environments which differ in morphology, trophic level, pollution type and the ways in which possible changes may happen. The subject of this study is the cladoceran communities of three lakes completely different from one another from the point of view of their morphological characteristics (Table I) and their general features: Lago Maggiore, in which eutrophication factors change continuously in time, Lago d'orta, poisoned by copper and ammonia wastes, and Lago Trasimeno where eutrophication factors fluctuate from year to year depending on climatic and météorologie variations. TABLE I - Main morphological features of the three lakes. Surface Volume Maximum depth Mean depth Drainage basin Theoretical renewal time Lago Maggiore 22 km 2 37.5 km 3 37 m 76 m 6599 km 2 4 years Lago d'orta 8 km 2.3 km 3 43 m 7 m 6 km 2 8 years Lago Trasimeno 26 km 2.6 km 3 6.3 m 4.7 m 396 km 2 24 years KEYWORDS: Cladocera - Environmental changes - Population responses. ACKNOWLEDGEMENTS The authors wish to thank Dr. Piera Pandolfi for her precious collaboration and Prof. Sandra Spence for revising the English manuscript. Prepared for presentation at the Symposium «Acque Interne ehe cambiano: la risposta délie comunità animali», organized by Prof. Giuliano Bonomi for the 54th Congress of the Unione Zoologica Italians, Perugia, September 28-October 3, 992. Lago Maggiore, located between Piedmont (Italy), Canton Ticino (Switzerland) and Lombardy (Italy), is a large subalpine lake of glacial origin which until recently was affected by human eutrophication problems, now partly solved due to treatment plants located mostly on the Piedmont and Swiss sides. Lago d'orta is also a glacial lake, located entirely in Piedmont territory, and is now in a phase of slow recovery after sixty years of heavy industrial pollution. Lago Trasimeno, in the Perugia district, is a wide shallow lake of tectonic origin, whose level may drop below the outflow threshold during years

386 BONACINA C, DE BERNARDI R., TATICCHI M. I. of scanty rainfall: in these circumstances the lake may remain without its effluent even for several years. CASE HISTORIES 5 4 3 + nfl Downloaded by [48.25.235.26] at 7:56 8 February 26 Lago Maggiore Baldi (95a, b) postulated for Lago Maggiore a high degree of stability in the plankton community. Indeed, the lake remained substantially unchanged from the beginning of the century till the sixties, as regards both trophic level and biocenotic structure (Tonolli, 962; Bonacina, 977). From the end of the sixties the lake was affected by progressive eutrophication, which reached its maximum at the end of the seventies: P tot rose from 4-6 to 37 ug I" (Mosello, 989) and chlorophyll a and algal biomass values rose at the same time (Ruggiu, 989). The beginning of the eighties saw the start of an oligotrophication process (about a 7% reduction in total P loading, with maximum values of 9% in the Swiss part of the basin and a minimum of 2% in the Lombard part), so that mean concentration values for P tot dropped to 5-6 ug I" (Calderoni et al., 992a, b). In spite of this, Lago Maggiore showed great environmental resilience, and it is only in the last three-four years that we have been able to note some community structure changes, such as an increase in specific diversity and a lowering of algal biomass (Ruggiu et al., 992). During the eutrpphication phase, the fish community was formed of huge populations of pelagic planktivorous fish; at present, the mean annual catch is about 5 tons, whereas at the beginning of the seventies it was one tenth of this value, with practically the same catch effort (unpublished data). Since 948 the Istituto Italiano di Idrobiologia has collected Zooplankton samples using the same methods and instruments, so that all data are comparable; moreover, since 98 sampling has been performed monthly. The most common pelagic species in the cladoceran community of Lago Maggiore are the filterfeeding Daphnia hyalina, Bosmina coregoni and Diaphanosoma brachyurum and the predators Leptodora kindtii and Bythotrephes longimanus. However, Chydorus sphaericus, Alona a/finis, Syda cristallina and Alonella excisa are also found sporadically. The cladoceran density trend closely follows that of P tot concentration (Fig. ). This is justified mainly by variations in the densities of D. hyalina (Fig. 2), which became the most important cladoceran species from the end of the sixties onwards, replacing D. brachyurum (Fig. 2), whose density continues to decrease despite yearly fluctuations. The third filter-feeding pelagic cladoceran living in Lago Maggiore, B. coregoni, was practically negligible until the end of the seventies but is now one of the major components of the community (Fig. 2). Of the two predator species present in the lake, namely L. kindtii and B. longimanus (Fig. 3), the more important as 5 tu 2 3 2 D o3 <r in iß CT> O3 CT5 g g I = TP D RP i a a D D a il! -- T- r- o S; S C f- 955 965 975 985 995 a B a H T? " " B n C u a a n ^ Fig. - Mean annual cladoceran densities (A, ind./m 3 ) and mean concentrations of Total Phosphorus and Reactive Phosphorus (B, ug I" ) in Lago Maggiore. regards both density and role is undoubtedly Leptodora though Bythotrephes has appeared in recent years to be assuming increasing importance in the community. Different factors regulating the population dynamics of each species can be recognized, such as: - food resources and consequently more or less severe competition, which could partly explain the greater success of Daphnia and Bosmina in comparison with Diaphanosoma; - prey-predator relationships, both among fish fauna on one hand and Daphnia, Leptodora, Bythotrephes on the other, and among filter-feeding species on one hand and Leptodora + Bythotrephes on the other; - factors depending on the seasonal meteorological cycle, which could explain the year-to-year variability. The fact that Bosmina densities have risen in the last few years may be due to lack of prédation on this species, which is not selected by any of the planktivorous fish living in Lago Maggiore (Giussani, 974). On the other hand fish prédation seems to play an important role in Daphnia dynamics, as might be demonstrated by its observed huge reduction in size (Manca, pers. comm.) and the simultaneous increase of the planktophagous fish population (planktophagous fish mostly select individuals of larger size, Brooks & Dodson, 965; de Bernardi, 974; de Bernardi & Giussani, 974; Zaret, 98). Invertebrate {Leptodora and Bythotrephes) prédation is responsible for the summer collapse of Daphnia: affect- "" n B

RESPONSES TO ENVIRONMENTAL CHANGES IN CLADOCERA 387 Downloaded by [48.25.235.26] at 7:56 8 February 26 3 2 8 JS^ 6 g 4 2 6 2 -> 8 -a s 4 Dspba/a. I l il Illlllll. r r r c o CTlCT3 O3 O3 Diapbanosoma bracbyurvm Bosmina coregoni * -^r r- es CO CO CO C^> O3 O3 O3 O3 Fig. 2 - Mean annual densities (ind./m 3 ) of the filter-feeding cladocerans in Lago Maggiore. 35 3 25 2. 5 ' Bytbotrepbes long im anus CO C73 t Leplodora kindlii Fig. 3 - Mean annual densities (ind./m 3 ) of the predator cladocerans in Lago Maggiore. ļ ing, as it does, chiefly the young, it practically eliminates the possibility of a population renewal. On the other hand, fish act mainly as a control factor of the spring peak, because in this period they prey chiefly on adult Daphnia (Mordukay-Boltovskaya, 958; de Bernardi, 974; de Bernardi & Giussani, 975). Lago d'orta From 927 onwards, Lago d'orta underwent a series of well-known vicissitudes (an exhaustive treatment of this subject and a full bibliography may be found in Bonacina & Bonomi, 984): around the end of the twenties, copper and ammonia wastes from a rayon factory disrupted the whole food-web and made the lake almost completely lifeless (Monti, 93). This situation went on for over fifty years; total inorganic nitrogen + copper loadings (input peaks of 335N y" and 9.5 t Cu y" were reached in 97, Bonacina & Bonomi, 985) resulted in concentrations in the lake water (mean annual values weighted for the height of water column) of 6.3 mg N-NH 4 r', 6.7 mg N-NO 3 T, 53 ng Cu r during full circulation time, March, 97 (Barbanti et al., 972; Mosello et al, 986). The huge quantity of nitrate nitrogen was of autochthonous origin, because nitrates are the final product of ammonia oxidation reaction, which also caused a marked drop in ph (3.9 average weighted value, at the overturn 985, Calderoni et al, in press). This result was to be expected, given the very low buffer capacity of the waters of Lago d'orta, whose drainage basin is almost completely granitic. At the beginning of the eighties, the lake began to make a slow and partial recovery (Bonacina & Bonomi, 984): in fact, the rayon factory implemented a treatment plant which greatly reduced the annual ammonia nitrogen loading (down to less than / of the maximum loading, Bonacina et al., 988). Finally in 989-99 a liming intervention was performed on the lake (Bonacina et al., 988; Calderoni et al., 99a) with the aim of lowering the abnormal acidity deriving from ammonia oxidation and the very low buffer capacity of the lake; this procedure would make it possible to further enhance the oxidation process, inhibited by low ph values, and, as a consequence, the lowering of ammonia nitrogen concentrations (volume weighted mean value at the overturn 992: 9 lxg N-NH 4 I", Calderoni et al, in press). Cladocerans in Lago d'orta were originally represented by Daphnia longispina, D. hyalina, D. galeata, D. pulex, Diaphanosoma brachyurum, Bosmina longirostris, Syda cristallina, Leptodora kindtii (Pavēsi, 879); this complex community reacted in a different way to each of these events. At the onset of pollution, it completely disappeared, due to the combined effects of toxicity and the failure of phytoplankton, which represents the only food resource for almost all species (Baldi, 949). Afterwards, an unbalanced biological community laboriously re-formed, represented by only one

388 BONACINA C, DE BERNARDI R., TATICCHI M. I. copepod species, some occasional rotifer species and very few phytoplankton species, whereas cladocerans were still absent (Bonacina, 97). This situation was to change radically as a result of the drop in ammonia nitrogen loading: starting from September 986 a stable population of Daphnia obtusa appeared in the lake (Bonacina et al., 988). Although it is known as a littoral species, it colonized the pelagial of the lake and is still present albeit with noticeable fluctuations in density. A very interesting feature is that this population is composed of individuals which are identical, that is, only one genotype is present, exactly the same for the 34 individuals studied (Bachiorri et al, 99), in spite of the presence of males which sometimes form up to 35% of the population (Fig. 4). In 987, with ph values around 4.5, N-NH 4 concentrations of.5-2 mg "', N-NO 3 concentrations of 3.5-3.9 mg T (Mosello, pers. com.), the cladoceran community was composed of D. obtusa and very few Chydorus sphaericus (Table II). As had been predicted (Bonacina et al., 988; % i "\ ļ^mm ESS RS5SH Downloaded by [48.25.235.26] at 7:56 8 February 26 5% % Fig. 4 - Percentage of different stages of D. obtusa (Y, young; M, mature females; O, ovigerous females) and of males (rf) in Lago d'orta during 987. TABLE II - Cladoceran densities (ind/m 3 ) in Lago d'orta during 987. Jan Feb Mar Apr May Jun Jul Aug Sep m o DM Y Oct Nov Dec Daphnia obtusa Chydorus sphaericus 34 629 2 258 2 76 3 32 3 534 5 2967 4537 4 429 9 582 9 3336 258 TABLE III - Cladoceran densities (ind/m 3 ) in Lago d'orta during 99. Jan Jan Feb Mar Apr Apr May Jun Jun Jul Aug Sep Nov Daphnia obtusa Daphnia longispina Bosmina longirostris Chydorus sphaericus Diaphanosoma brachyurum 388 258 3 72 3 2734 49 52 363 67 2 3 3 39 4 93 6354 4 4 85 2877 3 2

Downloaded by [48.25.235.26] at 7:56 8 February 26 RESPONSES TO ENVIRONMENTAL CHANGES IN CLADOCERA Calderoni et al., 99), the liming operations, which started in May 989 and ended in June 99 (Calderoni et al., 99a), enhanced ammonia oxidation, lowered its concentration, and increased ph; nitrate nitrogen concentrations, on the other hand, remained fairly constant (Calderoni et al., 99b, 99 and in press): in fact, nitrate nitrogen flows out of the lake in the effluent waters, but its concentration does not decrease because of the continuous nitrate production via ammonia oxidation. The community response to this evolution of hydrochemical conditions has been complex: some other cladoceran species have appeared in the lake (Daphnia longispina, Ceriodaphnia pulchella, Bosmina longirostris, Diaphanosoma brachyurum), albeit with very low densities except for Bosmina (Table III). The D. obtusa population seems to have decreased and its annual cycle been modified: in this case, a main factor may be the appearance in the pelagic water of a fish which is planktivorous in its juvenile stages (perch, Perca fluviatilis), whose prédation activity might have caused LAKE ORTA -Zooplankton- V in» ķ&ratemaoitûsfrats ccchteans tomjspiria ChydofifäJigh Osphpm vbtu. ßü mirt% tongirostris AsplarKhr>ā brtohtw*ifļ 97 975 98 985 99 cfria îstractis ns floxïïis longirminus Fig. 5 - Scheme of increasing enrichment of zooplanktonic community in Lago d'orta. 257.33 m o 984 985 986 987 988 989. 99. 99 Fig. 6 - Daily surface level variations of Lago Trasimeno in 984-99. 389 the lowering of Daphnia density. On the other hand, the reduced competition could explain (de Bernardi & Giussani, 978; de Bernardi & Soldavini, 979) the noticeable peak of Bosmina population (more than 6, ind. rrf 3 in November). A synoptic graphic representation of the increasing complexity of the Zooplankton community as a whole is given in Figure 5. Lago Trasimeno Lago Trasimeno is prevalently fed with rain water so that its chemical characteristics are strictly dependent on climatic and meteorological conditions. From 984 to 988 the lake level was almost always above the outflow threshold (Fig. 6). From 989 to 99 it remained below the threshold. Chemical and physical parameters are significantly correlated with lake water level (Gianotti et al, 982; Tiberi, 985; Mearelli et al., 99). In years with scanty rainfall nitrates are not washed away from the cultivated catchment area, so that nitrate concentrations in the lake waters decrease (precipitations: 987 = 7.47 mm; 988 = 59.95 mm; 989 = 47.7 mm; 99 = 52.3 mm; 99 = 76.3 mm. N-NO 3 concentrations: 987-988 =.8 mgr ; 989 =.7 mgt ; 99 =.4 mgt ; 99 =.6 mg r'); at the same time the high summer evaporation results in an increase of chloride and sulphate concentrations. The food chain as a whole showed the effect of these variations in level: as was observed by Mearelli (985), there is a close relationship in Lago Trasimeno between lake level and variations in fish production. In the three years 989-99-99 an important reduction offish catch is evident (293, 37, 243 tons, respectively) if compared with values for 986-987-988 (56, 624, 42 tons), although the catch effort remained almost unchanged. It should be noted that the ratio between various species changed: for example, Atherina boyeri, a species which is planktivorous for the whole of its life, represented about 28% of the total fish catch during the period 986-988 but only 3% during 989-99; on the other hand Scardinius erythrophthalmus, which feeds on Zooplankton only in the very early stages (summer months) increased in the same period from 3 to 34%. Pelagic Zooplankton has been sampled continuously from 987 to the present. The cladoceran community in the years 987-99 is composed of six species (Table IV): Bosmina longirostris and Daphnia galeata are clearly dominant every year; D. brachyurum and L. kindtii are prevailingly summer species and are present only for a very limited period of time; Daphnia cucullata, once very abundant in the lake, is now to be considered as sporadical (some individuals were sampled in June 989 and May 992, not shown in the table); finally Ceriodaphnia pulchella has apparently been absent since 988. The composition and density of the cladoceran com-

39 BONACINA C, DE BERNARDI R., TATICCHI M. I. munity clearly change with the lake level: from 987 to 99 an increase of B. longirostris and a decrease of D. galeata were observed (Fig. 7) as regards both density and duration of presence. In the rainy year 99 the two species partly re-balanced: indeed there is a highly significant inverse correlation between their densities. The factors regulating the population dynamics of the two main species during the study period are essentially: - fish prédation in 987-988; the effect of prédation pressure is particularly evident in Daphnia, which shows a decrease in mean size at the time of first maturation during 987 and a decrease in mean individual size during 988 (Fig. 8; Taticchi et al, 989). It is interesting to note that Bosmina shows the greatest mean size in the same period. Gut content inspections of A. boyeri demonstrated that it selected both Bosmina and Daphnia equally; - quality and quantity of available food in 989-99; in this period there was not only a decrease in the importance of fish prédation in the lake (the fish catch drastically decreased without a corresponding decrease in catch effort), but also a shortage of food, with ultraplankton making up more than 5% of the total density of phytoplankton). A competition interaction is becoming established between the two dominant species, which rely on similar trophic resources; in these conditions Bosmina is better able to exploit the available food. In fact, Daphnia devotes all its available energy to egg production, but at hatching the newborns will not have enough food while Bosmina, whose embryonic Downloaded by [48.25.235.26] at 7:56 8 February 26 TABLE IV - Cladoceran community composition in Lago Trasimeno during the period 987-99-, presence;, scarcity;, abundance. Bosmina longirostris Daphnia galeata Daphnia cucullata 987 988 989 99 99 987 988 989 99 99 987 988 989 99 99 M M O D Diaphanosoma brachyurum 987 988 989 99 99 Leptodora kindtii 987 988 989 99 99 Ceriodapbnia pulcbella 987 988 989 99 99

RESPONSES TO ENVIRONMENTAL CHANGES IN CLADOCERA 39 s g ļ s s ļ =. =. i. ä. ' " ' \. Im im. 987 988 989 99 99 987 988 989 99 99 Fig. 7 - Population density (ind. "') of B. longirostris (A) and D. galeata (B) in Lago Trasimeno for the period 987-99 (note the log scale). u Downloaded by [48.25.235.26] at 7:56 8 February 26 development time is shorter, is able to reduce its birth rate and maintain the original mean individual length of the population and high density values. On the contrary Daphnia, especially in 99, showed a further reduction of mean length and a low population density; - the rainfall in 99; even though the lake level has not shown any significant variation, the trophic level is tending to increase and the phytoplankton composition is changing: ultraplankton is now only 34% of the total phytoplankton, chlorophycean density has almost doubled, algal blooms typical of Lago Trasimeno {Phormidium, Anabaena, Nostoc, Dinobryon, Tetraedron, Ankistrodesmus, Ceratium) are appearing and total phytoplankton biomass is increasing, so that Daphnia may once more be successful in its competition with Bosmina (Taticchi, 992). CONCLUDING REMARKS Cladoceran populations seem to have a good stability (meaning by «stability» the persistence of the same species in the same community) in relation to gradual environmental changes which happen without marked discontinuities. This is the case in Lago Maggiore, in which each specific entity returns each time to a situation of equilibrium, adapting itself to changing environmental conditions without any great rearrangement of the taxonomic composition. In a great lake like Lago Maggiore, with its considerable inertia, environmental changes may be absorbed by a species by the expedient of, for example, modifying its spatial position, so avoiding a fundamentally harmful event such as that of mass transport coming from a flooding tributary (Ambrosetti et al, 98) or increased prédation and/or competition (de Bernardi & Soldavini, 98). When environmental conditions show a catastrophic trend, the community structure is severely affected, to the extent of complete disappearance, as was the case in Lago d'orta where the present community is composed of species which have replaced and will in turn be 35-25 - 5 - - - 987 -ļ i i 8-i 4-3- 2-5- 6-4- 2 U ^\ 987 i 988 989 99 99 i it i i i i ; rid. n d. 988 989 99 99 Fig. 8 - Mean individual length (black) and mean length of the primiparae females (dashed) of B. longirostris (A) and D. galeata (B) in Lago Trasimeno for the period 987-99 (n.d., not determined). replaced by species typical of more advanced stages of the secondary succession'deriving from lake recovery. In this sense, D. obtusa is to be considered a pioneer species. Finally, when climatic factors rather than human impact produce drastic but not catastrophic environmental

392 BONACINA C, DE BERNARDI R., TATICCHI M. I. Downloaded by [48.25.235.26] at 7:56 8 February 26 changes, as in the case of the shallow Lago Trasimeno, which is devoid of environmental inertia, community structure itself is rapidly modified, because of its inability to tolerate the changes.- some species may be replaced by others (D. cucullata has been replaced by D. galeata, and the latter by B. longirostris); but succession may return to a previous stage when the former environmental conditions are restored. Nevertheless, with the exception of the second case considered, all the changes that can occur rely on similar biotic variations, such as an alteration in prey-predator relationships, food increase or decrease, variations in phytoplankton community structure etc. REFERENCES Ambrosetti W., Barbanti L., de Bernardi R., Libera V., 98 - Alcune tisposte limnologiche ad un evento meteorologico eccezionale: il nubifragio del 7 Agosto 978 nel bacino del Lago Maggiore. 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