Planktonic microcrustaceans (Crustacea: Cladocera, Copepoda) from several protected peat wetlands, differing in trophic state

NORTH-WESTERN JOURNAL OF ZOOLOGY 10 (Supplement 1): S78-S86 ©NwjZ, Oradea, Romania, 2014 Article No.: 140303 http://biozoojournals.ro/nwjz/index.html

<< Fauna of the Romanian protected areas - A special issue in memoriam of Acad.Dr.Doc. Petru M. Bănărescu >>

Planktonic microcrustaceans (Crustacea: Cladocera, Copepoda) from several protected peat wetlands, differing in trophic state

Karina Paula BATTES*, Iuliana MOLDOVAN and Alina SAS

Department of Taxonomy and Ecology, Babeş-Bolyai University, 5-7 Clinicilor Str., 400006, Cluj-Napoca, Romania.

*Corresponding author, K.P. Battes, E-mail: [email protected]

Received: 06. December 2013 / Accepted: 15. June 2014 / Available online: 20. November 2014 / Printed: December 2014

Abstract. The present paper represents an inventory of microcrustacean species from seven peat wetlands, representing oligotrophic, mesotrophic and eutrophic states: Tăul lui Dumitru, Tinoavele plutitoare de la Hoteni, Tinovul Mare Poiana Stampei, Mlaştina de la Iaz, Molhaşul Mare de la Izbuc, Tinovul Mluha and Tăul fără fund de la Băgău. Most of these wetlands are protected areas, except for Tinovul Mluha, whose characteristics of a typical peat bog offer strong arguments for future protection. A total number of 31 crustacean species were identified: 21 cladocerans and 10 copepods. Two distinctive clusters of the sampling locations were distinguished, based on microcrustacean presence/absence data: one ”true oligotrophic” group and an ”oligo-meso-eutrophic” group. The major abiotic factors influencing the qualitative structure of microcrustacean communities were pH and altitude. The microcrustacean communities from the ”true oligotrophic” group recorded higher equitability values, showing a more balanced diversity. The abundance variation of different functional groups of non-predatory cladocerans, carnivorous cladocerans and copepods suggested competition between the groups with similar food resources.

Key words: limiting factors, diversity, equitability, similarity, functional groups.

Introduction Marshes represent particular environments be-cause of their unique characteristics related to cli-mate, hydrology or pedology. Marshes with peat accumulations are a diverse and outstanding group of wetlands, supporting a peculiar biota, with special adaptations to limiting factors like food scarcity or high acidity. At the same time, peatlands represent the most valuable and threat-ened biotopes in Europe (Charman 2002).

Zooplankton communities occupy a central place in wetland food webs, regulating matter and energy flows from the primary producers to con-sumers of higher ranks (Wetzel 2001). Microcrus-taceans are the most numerous group of animals in planktonic assemblages, followed by rotifers and protozoans (Jasser et al. 2009). Cladocerans are mostly filter-feeders, gathering phytoplankton or detritus from the water column (Negrea 1983). Few species are predatory; unlike copepods, that are carnivorous even as immature stages (copepo-dites) (Lampert & Sommer 2007).

The incredible diversity of peat wetland types is reflected in the multitude of terms used to de-nominate the different types. For example, the seven peat wetlands considered for the present paper differ in nomenclature: the oligotrophic ones are called ”tău”, ”tinov” or ”molhaş”, equiva-

lents to the English term ”bog”, while the eutro-phic one is called ”mlaştină”, meaning freshwater marsh. Eutrophic marshes are formed on satu-rated anaerobic substratum, rich in nutrients com-ing from percolating waters. They are found at dif-ferent altitudes, with a characteristic flora of water mosses, macrophytes, or trees (Phragmites, Typha, Scirpus, Juncus, Carex, Glyceria, Dryopteris, Equise-tum, Potentilla, Salix, Alnus, Rhamnus, Betula, Popu-lus etc.). Usually the peat layer is formed under the infiltration water. Oligotrophic marshes on the other hand, have a very distinctive aspect, with a curved surface where depressions in the peat layer are filled with water. These marshes are only found in humid and cold climates, at altitudes ranging from 500 to 1200 m a.s.l. (Pleniceanu 2003). Being isolated from the soil, the biotic communities living here must rely solely on nutri-ents coming from precipitation waters. The typical vegetation is dominated by several moss species of Sphagnum. The diversity of oligotrophic wetlands is usually low, due to high acidity and the toxins released by Sphagnum (Pop 1960). The wetlands with intermediate characteristics are characterized as mesotrophic.

The present paper describes the microcrusta-cean communities from seven peat wetlands from Transylvania and Bucovina: Tăul lui Dumitru, Ti-noavele plutitoare de la Hoteni, Tinovul Mare

Planktonic microcrustaceans from several protected peat wetlands

S79

Poiana Stampei, Mlaştina de la Iaz, Molhaşul Mare de la Izbuc, Tinovul Mluha and Tăul fără fund de la Băgău. Secondly, the study examines the main trends of the microcrustacean functional groups: filter-feeding and predatory cladocerans of differ-ent sizes, and copepods; in relation with abiotic factors.

Previous studies on planktonic microcrusta-ceans from the seven sampling locations are scarce. Pop (1960) described in detail the peat wet-lands from Romania, with both abiotic and biotic characteristics, however he gave no information on planktonic microcrustaceans. Zoological re-cords regarding plankton communities were based solely on protozoans and rotifers. Similarly, Negrea (1962) did not mention any of the seven sampling locations in his analyses, so there are no citations of cladoceran species before 1960. Pleşa (1958) only cited the presence of Megacyclops viri-dis in a Sphagnum waterpool from the Padiş Pla-teau, the Apuseni Mountains, that could be within the area of Molhaşul Mare de la Izbuc. Finally, none of the seven sampling locations were found in more recent literature (Forró & Kovács 2008).

Thus, the present study helps fill the gaps of the microcrustacean inventory in several peat wet-lands from Transylvania and Bucovina, as well as elucidating the main limiting factors and the variation of crustacean functional groups in these special habitats. Material and methods Seven sampling locations were considered for the present study, numbered from 1 to 7 (Table 1, Fig. 1). The sam-plings took place in late spring and summer between 2010 and 2013. In three locations, more than one sample were collected, so the codes used to denominate the samples were constructed accordingly. Thus, a site is encoded firstly by its location; letters a, b or c refer to different col-lection places within one location and the last figures re-fer to the sampling date (e.g. 5.12 means May 2012) (Table 2).

“Tăul lui Dumitru” (Fig. 2, Table 1) is a typical oligotrophic peat bog, with a surface area of 6–7 ha (the peat bog itself 3 ha), the mean peat layer thickness is 5.5 m (Pop 1960).

Pop (1960) described “Tinoavele plutitoare de la Ho-teni” (Table 1) as a true oligotrophic bog, having an elon-gated shape, 550 m long and 40 m wide. The peculiarity of this bog is that the peat layer of about 2.5 m thick is floating on a water stratum, 4 m deep (Chiş 2007). The flora from this region is diverse, including not only oligotrophic species but also typical eutrophic ones (Ho-tea et al. 2003-2004).

With a large surface area, exceeding 690 ha, “Tinovul Mare Poiana Stampei” represents an important active and forested peat bog, with a peat layer of 2–4 m thick and a peat volume of 6000000 m3 (Pop 1960). The biological samples were collected from a small and shallow water body located on a creek near the access path.

“Mlaştina de la Iaz” (Fig. 3) has a total surface area of 10 ha and a maximum depth of 5 m. Pollen analyses showed that the peat layer started to accumulate in this region 8000 years ago (Coldea 1971). The marsh is sur-rounded by forests (Fagus, Quercus, Alnus), but the wet-land is characterized by a meso-oligotrophic vegetation. Five Sphagnum species were identified within the pro-tected area, together with numerous habitats of national and European value, ranging from natural dystrophic lakes, transitional peat bogs (mesotrophic marshes), to meads and forests.

“Molhaşul Mare de la Izbuc” is a typical oligotrophic bog, surrounded by spruce (Picea). It has a surface of 8 ha, with an elongated shape and more than 20 small water bodies with a surface area ranging from 1 to 5 m2. The peat layer has a thickness of about 4 m and a volume of 320000 m3 (Pop 1961).

“Tinovul Mluha” is a typical oligotrophic peat bog, similar to those from the Someşul Cald and Someşul Rece River Valleys, however isolated from them, being located in the Arieş catchment area. The peat bog has a total sur-face area of 10 ha; the peat layer has a thickness of more than 7 m in the middle and a volume of 450000 m3 (Pop 1960). Tinovul Mluha is not currently a protected area, but its presence in the present paper was motivated by its special features of a typical peat bog.

“Tăul fără fund de la Băgău” includes a lake, but also a eutrophic marsh, of about 3 ha in the eastern part of the water body, with a 0.7–0.8 m thick peat sediment, floating on a deep water layer (Pop 1960). There is also a small oligotrophic area of 0.8 ha.

Several physical and chemical parameters (pH, dis-solved oxygen, water temperature) were measured in the field, using portable meters (Consort P902 for pH and YSI 52 for dissolved oxygen).

Qualitative samples of microcrustaceans were taken, using a 55 µm mesh zooplankton net. All samples were collected from the banks of the water bodies and pre-served in 4% formaldehyde. Crustaceans were identified to the species level, using the available literature for cladocerans (Negrea 1983) and copepods (Damian-Georgescu 1963, 1970; Einsle 1993). The validity of the taxa was checked in the Fauna Europaea database (de Jong 2013). Immature copepods - copepodites and nauplii - are impossible to identify to the species level, so they were included in the statistical analyses as distinct cate-gories. Planktonic rotifers, as well as different benthic groups were also found in the samples, but were not in-cluded in the analyses.

The similarity between the microcrustacean commu-nities from the sampling sites was calculated using the Dice index (Dice 1945), which only uses qualitative data (presence/absence of the taxon). Semi-quantitative esti-mations were carried out for all the sampling sites, by cal-

K.P. Battes et al.

S80

Table 1. Main characteristics of the seven sampling locations.

Locationcode

Location name

GPS coordinates

Altitude(m a.s.l)

Geographical position

Protection status (Brînzan 2013)

Character

1 Tăul lui Dumitru

47°49’26.5”N, 23°42’01.9”E

1146 The Eastern Carpathians Ecoregion, Maramureș

county

Natural monument (IUCN protected areas - category

III); ROSCI0092 Igniş

Oligotrophic

2 Tinoavele plutitoare de la

Hoteni

47°45’50.4”N, 23°54’24.4”E

528 The Eastern Carpathians Ecoregion, Maramureș

county

Natural monument (IUCN protected areas - category III)

Oligotrophic

3 Tinovul Mare Poiana Stampei

47°17’42.32”N,25°07’01.3”E

919 The Eastern Carpathians Ecoregion, Suceava county

ROSCI0247 Tinovul Mare Poiana Stampei

Oligotrophic

4 Mlaştina de la Iaz

47 ̊06’38.3”N, 22 ̊ 39’39.8”E

320 The Western Carpathians Ecoregion, The Apuseni Mountains, Sălaj county

Nature reserve (IUCN protected areas - category IV)

Mesotrophic

5 Molhașul Mare de la Izbuc

46°35’33.4”N, 22°45’42.2”E

1204 The Western Carpathians Ecoregion, The Apuseni Mountains, Bihor county

ROSCI0002 Apuseni Oligotrophic

6 Tinovul Mluha 46°19’52.4”N, 23°20’13.6”E

1336 The Western Carpathians Ecoregion, The Apuseni Mountains, Alba county

- Oligotrophic

7 Tăul fără fund de la Băgău

46°19’50.7”N, 23°48’29.8”E

427 The Transylvanian Plateau Ecoregion, Alba county

ROSCI0004 Băgău Eutrophic

Figure 2. A typical peat bog: Tăul lui Dumitru, sampled in July 2011

Figure 3. A typical mesotrophic wetland: Mlaştina de la Iaz (code 4b-7.12), sampled in July 2012.

Figure 1. Locations of the seven peat wetlands sampled in the

present study: 1. Tăul lui Dumitru,

2. Tinoavele plutitoare de la Hoteni, 3. Tinovul Mare Poiana Stampei,

4. Mlaştina de la Iaz, 5. Molhaşul Mare de la Izbuc,

6. Tinovul Mluha, 7. Tăul fără fund de la Băgău)


S81

culating the relative percentage abundance. A certain number of individuals was counted in each sample, rang-ing from 58 to 160, and the percentage of the species pre-sent was calculated. These semi-quantitative data were used to express the biological divesity, based on the Shannon-Wiener Index and on Equitability (Washington 1984). The Principal Component Analysis (PCA), one of the most frequently used multivariate data analysis methods (Jolliffe 1986), was performed in order to visual-ize the sampling locations depending on several vari-ables: both abiotic (water temperature, dissolved oxygen, pH, altitude), but also biotic variables (abundance of fil-ter-feeding cladocerans, carnivorous cladocerans, adult and immature copepods, expressed as sum of individuals in each sampling location). Equitability was also consid-ered. Significant correlations were tested using the linear Pearson test. Statistical analyses were performed using PAST (Version 2.14-2012) and XLSTAT (Evaluation ver-sion 2013.5). Results The main physical and chemical parameters were recorded in the seven sampling locations (Table 2). The highest pH values were recorded in the mesotrophic marsh Mlaştina de la Iaz, while in the rest of the sampling locations acidic conditions prevailed. Dissolved oxygen recorded relatively high values, except for the hypoxic conditions from the same marsh in May 2012. Water tempera-tures were normal for late spring and summer.

A total of 21 cladoceran taxa were found in the seven locations, while only 10 cyclopoid and har-pacticoid copepods were identified, together with their development stages: copepodites and nauplii (Table 3). The cosmopolitan cladoceran Chydorus sphaericus was the only species present in all sam-pling locations. Other microcrustaceans were fre-quent in most of the sampling locations, usually eurybiotic species like Alonella excisa, Scapholeberis mucronata, Simocephalus vetulus, Streblocerus serri-caudatus or the copepods Eucyclops serrulatus proximus, Megacyclops viridis or Thermocyclops dy-bowskii. On the other hand, five microcrustacean species were recorded only from Mlaştina de la Iaz, some indicatative of a high organic load, like the copepod Cyclops strenuus that lives in beta-alpha mesosaprobic waters according to Sládeček (1973). Three microcrustacean species were spe-cific for the peat bog Molhaşul Mare de la Izbuc: the filter-feeder Ceriodaphnia quadrangula var. ha-mata, the carnivorous cladoceran Polyphemus pedi-culus and the copepod Diacyclops nanus, known to live in dystrophic conditions. The harpacticoid co-pepods were specific to moss habitats (Bryocamp-

tus abnobensis and Elaphoidella gracilis). An empiri-cal evaluation of the frequency of appearance was performed for all the taxa identified in the sam-pling location, on a ranking scale ranging from r (rare) to d (dominant) (Table 3).

Other organisms were present in the samples, due to the collection technique: rotifers (As-planchna, Brachionus, Keratella, Lecane, Polyarthra, Trichocerca), nematodes, oligochaetes, dipterans (chironomids, chaoborids, culicids), caddisflies, dragonflies, coleopterans, hemipterans, mayflies, ostracods and water mites.

The similarity between the microcrustacean communities based solely on the presence or ab-sence of the species is presented in Figure 4. Two clades are differentiated in the cluster analysis. On the one hand, there is the ”true oligotrophic” group, including the typical peat bogs: sampling locations 1, 5 and 6 (Tăul lui Dumitru, Molhaşul Mare de la Izbuc and Tinovul Mluha). Quite dif-ferent is the ”oligo-meso-eutrophic” group, com-prised of not only the non-oligotrophic marshes: 4. Mlaştina de la Iaz and 7. Tăul fără fund de la Bă-gău, but also of two special cases of oligotrophic wetlands: 2. Tinoavele plutitoare de la Hoteni, where eutrophic elements appeared in recent years; and 3. Tinovul Mare Poiana Stampei, where sampling took place on a small shallow creek from the peat bog, not the most characteristic water body.

Species richness (the number of taxa present in the samples) showed a similar pattern to the di-versity index (Fig. 5), meaning that the higher the number of taxa, the higher the diversity. However, there are two cases of inverse variation: in Ti-noavele plutitoare de la Hoteni, Alona rectangula recorded a high number of individuals while in Mlaştina de la Iaz, Daphnia curvirostris dominated the microcrustacean community, thus lowering the equitability and, in turn, the biodiversity.

Figure 6 presents the PCA biplot that aggre-gated the seven sampling locations depending on several important factors. Abiotic parameters var-ied in the wetlands considered for the present study: pH had higher values in locations 4 and 7 (Mlaştina de la Iaz and Tăul fără fund de la Bă-gău), while the highest altitude was characteristic to the typical peat bogs: 1, 5 and 6 (Tăul lui Dumitru, Molhaşul Mare de la Izbuc and Tinovul Mluha) (Fig. 6). Predatory cladocerans (Polyphemus pediculus) were only found in location 5 (Molhaşul Mare de la Izbuc), where copepods were not very abundant. Equitability and the Shannon-Wiener

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K.P. Battes et al.

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Figure 5. The number of taxa identified for all sampling locations (nauplii and copepodites included)

and the Shannon-Wiener index (sampling site abbreviations as in Table 2) index have the same variation, and they were negatively correlated with the pH values and di-rectly correlated with the altitude (Pearson corre-lation between pH and the Shannon Wiener index, r = -0.701, p = 0.0163; Pearson correlation between altitude and the Shannon Wiener index, r = 0.693, p = 0.018).

Discussion The microcrustacean species identified in the seven peat wetlands belonged to two major cate-gories. Firstly, there were the ”true oligotrophic” species, mainly rare and oligosaprobic taxa, indi-cating the nutrient scarcity of these habitats. The second ”oligo-meso-eutrophic” group, a more het-erogeneous one, included cosmopolitan and eury-

Figure 4. The similarity between microcrustacean communities from the seven sampling locations according to Dice index (nauplii and copepodites included) (sampling site abbreviations as in Table 2).


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Figure 6. Principal Component Analysis (PCA) biplot of the seven sampling locations (abbreviations as in Table 2) and their aggregation based on the following factors: pH, water temperature (WA.TE), altitude (AL), dissolved oxygen (DO), small cladocerans (SM.CL), large cladocerans (LA.CL), predatory cladocerans (PR.CL), adult cope-pods (AD.COP), immature copepods (IM.COP) and community equitability (EQ).

biont species, some of them indicating beta to al-pha mesosaprobic conditions (higher organic mat-ter loads).

The number of taxa identified in the 7 peat wetlands is comparable to other findings in the lit-erature: van Duinen et al. (2003) found 17 clado-ceran taxa and 6 copepod taxa in both natural and restored raised bogs in the Netherlands; Sharma & Bhattarai (2005) found 13 taxa of cladocerans and 3 taxa of copepods in a peat bog from Bhutan.

Thus, the low species richness characteristic to peat bogs (Cosentino et al. 2004) is clear in all sam-pling locations: no sampling location recorded more than ten microcrustacean species, because of the peculiar habitat conditions of high acidity, that acts as a limiting factor. Stressful conditions were common to the mesotrophic marsh too (Mlaştina de la Iaz), since gamogenetic females were found in high abundance in May 2012. The limiting fac-tor however was not acidity, but the drastic drop of water levels due to drought. In fact, diversity of peat wetlands is much debated in the literature. Hannigan & Kelly-Quinn (2012) cite a total of 137 macroinvertebrate taxa found in different peat-lands, ranging from deep pools to drought-sensitive Sphagnum hollows, with higher diversity related to higher habitat heterogeneity. Štěpánk-ová et al. (2012) found a rich desmid flora in sev-eral peat bogs from the Jeseníky Mountains, east-ern Czech Republic, but the species richness ranged from 4 to 21 desmid taxa in the sampling sites.

In spite of the low number of taxa, microcrus-

tacean diversity from the seven sampling locations recorded values comparable to those in other freshwater environments, due to high equitability. ”True oligotrophic” water bodies are located at higher altitudes and are very acidic (low pH val-ues), but they are balanced with respect to the number of individuals in each taxon, so they have high equitability values. These results agree with data from the literature: in naturally acidic waters, a healthy zooplankton community develops, which can out-number phytoplankton, inspite of the fact that zooplankton diversity decreases with increasing acidity in most freshwater environ-ments (Holland et al. 2012). Similar findings, with moderately high diversity and high evenness, were cited by Sharma & Bhattarai (2005).

The altitude and the pH represented the most important abiotic factors that differentiated the 7 peat wetlands considered for the present paper. Other studies showed that water temperature can affect the entire food web of a peat bog (Quiroga et al. 2013). However, that was not the case here, since samples were taken in late spring and sum-mer, when water temperature did not record a high variation. Clear patterns were depicted for several functional groups within the microcrusta-cean communities. The vast majority of cladoceran species are filter-feeders (Negrea 1983), regardless of their size. We considered large cladocerans as those exceeding 700 µm in total length. There are a few carnivorous cladoceran species, with one found in Molhaşul Mare de la Izbuc. As for cope-pods, most of them are efficient predators, feeding

K.P. Battes et al.

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mostly on protozoans and rotifers, but also on small cladocerans or algae in their later develop-ment stages and as adults (Dussard & Defaye 2001). The abundance of these functional groups recorded a divergent variation along the seven sampling locations. Small cladocerans are in-versely correlated to large ones, because they compete for the same food resources: algae and detritus. When large ones are abundant, the small ones record lower numbers. Predatory cladocerans compete for the same prey with copepods, so they too are inversely correlated.

In conclusion, the present study brings new data on the microcrustacean fauna from seven peat wetlands, all poorly studies with respect to these animal taxa. The qualitative composition and diversity of microcrustacean communities were influenced by the trophicity of the waterbod-ies, pH and altitude, with a higher, more ”bal-anced” diversity in the high-altitude acidic ”true oligotrohpic” marshes, while abundance varia-tions of microcrustaceans might be considered evidence for strong competition between different functional groups, with similar food resources in these nutrient poor environments.

Tinovul Mluha represents a special but vul-nerable habitat, a typical peat bog, whose unique features should be preserved as a protected area. Microcrustacean data included in this study sup-port this idea. References Brînzan, T. (ed.) (2013): Catalogul habitatelor, speciilor si siturilor

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Planktonic microcrustaceans (Crustacea: Cladocera, Copepoda) from several protected peat wetlands, differing in trophic state

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