Bhushan Kumar SHARMA, Shaikhul Islam KHAN, Sumita SHARMA

Freshwater Biology Laboratory, Department of Zoology, North-Eastern Hill University, Shillong-793 022, Meghalaya, India

1 INTRODUCTION

The floodplain lakes form an integral component of the major riverine systems world-wide. These wetlands attract attention as a lucrative source of inland fisheries and for rich aquatic biodiversity.These generalizations hold valid for the floodplain lakes (beels) of the Brahmaputra river basin of NEI(Sugunan, 1997; Sharma and Sharma, 2008, 2013)and those of lower Assam in particular. The latter are subjected to unplanned fishing with removal of aquatic vegetation thus altering their ecotone character. Referring to biodiversity value, Segers et al. (1993) firstly hypothesized tropical and subtropical floodplain lakes to be globally interesting habitats for the rotifer diversity. Sharma and Sharma (2008,2014a, 2014b) extended this hypothesis to the Brahmaputra floodplains of the Indian sub-region based on analysis of extensive plankton and semiplankton collections. The noteworthy reports of 171 and 162 rotifer species from Deepor beel (Sharma and Sharma, 2015a) and Loktak Lake (Sharma et al.,2016)—two Ramsar sites of India and important NEI wetlands, respectively hold distinction as one of the richest rotifer habitats. Rotifera, an integral link of aquatic food-webs, are also known to be useful bioindicators and thus useful to depict trophic status of water bodies (Sláde?ek, 1983).

Fig.1 Map of India showing Northeast India (NEI) and Assam state (green) (a); map of Assam indicating Barpeta district (b)

Realizing the rotifer biodiversity value of the Brahmaputra basin beels vis-à-vis the role of sampling, use of these metazoans to assess trophic status and to characterize habitat variations, we undertook limnological reconnaissance of four beels of lower Assam. Our study resulted in the detailed analysis of Rotifera assemblages with species-rich inventory of the taxon and interesting features. The nature and composition of the rotifer fauna are discussed with reference to biodiversity, distribution and ecosystem diversity, and various interesting rotifers are illustrated. Remarks are made on monthly richness variations, community similarities and on individual as well as cumulative influence of abiotic factors. We propose L/B quotient based onLecane:Brachionusspecies ratios to depict habitat variations and use B/T quotient (Sláde?ek, 1983) to comment on trophic status of the sampled wetlands.

2 MATERIAL AND METHOD

This study is a part of limnological survey of four floodplain lakes (26o17′08.7″–26o30′22.2″N;90o52′12.8″–91o02′43.1″E; altitude: 37.9–54.6 m ASL) namely Fingua, Baria, Sorbhog and Balaisuti beels of the Barpeta district of lower Assam, NEI(Fig.1a, b) undertaken during November 2011–October 2013.Eichhorniacrassipes(Mart.) Solms,Hydrillaverticillata(L. f.) Royle,PistiastratiotesLinnaeus.,SalviniacucullataRoxb.,Azollasp. andTrapanatansL. commonly occurred whileNymphoidessp.,Ipomoeasp.,Lemnasp.,Hygroryza aristata(Retz.) Nees,OryzarufipogonGriff . andNelumbosp. are other aquatic plants of these wetlands.These beels experienced habitat disturbances during intensive fishing from November-February with removal of aquatic vegetation and varying extent of unplanned fishing from January–October during each year.

Water samples were collected monthly from four beels and analyzed for ten abiotic factors. Water temperature, specific conductivity and pH were recorded in the field using relevant probes; Winkler’s method was used for estimation of dissolved oxygen and Greenberg (1992) was followed to analyze total alkalinity, total hardness, calcium and chloride. The rainfall data was obtained from local meteorological sources. The qualitative plankton samples were collected monthly from Fingua, Baria, Sorbhog and Balaisuti beels by towing a nylobolt plankton net (#50 μm) and were preserved in 5% formalin. Plankton samples were screened, individual rotifers were isolated and mounted in Polyvinyl alcohollactophenol, and were observed with Leica (DM 1000) stereoscopic phase contrast microscope using an image analyzer. Interesting rotifers were illustrated and measurements were given in micrometers (μm).The rotifers taxa were identified following Koste(1978), Segers (1995), Sharma (1998), Sharma and Sharma (1999, 2008, 2013). The community similarities were calculated vide S?rensen’s index and SPSS (Version 20) was used for hierarchical cluster analysis. Two-way ANOVA was used to ascertain significance of richness variations. The relationships between abiotic factors and richness were determined by Pearson’s correlation coefficients(R). The canonical correspondence analysis was done using XLSTAT (2015) to analyze cumulative influence of 10 abiotic parameters namely water temperature,rainfall, pH, specific conductivity, dissolved oxygen,free carbon dioxide, total alkalinity, total hardness,calcium and chloride on the rotifer richness.

Table 1 Variations in abiotic parameters of beels

We propose L/B quotient, based onLecane:Brachionusspecies ratios, to characterize habitat changes of the sampled beels. As per our results, L/B quotient values up to 1.0; 1.0–3.0; and above 3.0 categorized limnetic, semi-limnetic and littoralperiphytic habitat nature, respectively. Comments on trophic status of the beels are based on B/T quotient based onBrachionus:Trichocercaspecies ratios following Sláde?ek (1983).

3 RESULT

The variations (ranges, mean±SD) of ten abiotic factors are presented in Table 1. Water temperature varied between (26.9±5.1)–(27.2±5.1)°C, pH between(7.33±0.29)–(7.79±0.34) and specific conductivity between (122.3±38.5)–(372.0±80.1) μS/cm while dissolved oxygen and free carbon dioxide fluctuated between (4.0±0.5)–(5.1±0.6) mg/L and (11.3±6.6)–(23.0±10.6) mg/L, respectively amongst the sampled beels. The monthly rainfall, total alkalinity, total hardness, calcium and chloride ranged between(154.8±177.6)–(299.5±395.8) mm, (85.1±44.7–(186.3±95.4) mg/L; (52.2±9.3)–(164.8±59.6) mg/L;(28.7±11.8)–(94.9±31.1) mg/L and (12.8±3.6)–(18.5±7.8) mg/L, respectively.

A total of 160 species belonging to 19 families and 35 genera are observed from four beels of Barpeta,lower Assam (Appendix I).Cephalodellatrigona(Fig.2a) is a new record to the Oriental region;Lecane bifastigata(Fig.2b) is new to NEI; andTrichocerca hollaerti(Fig.2c),T.maior(Fig.2d) andDissotrocha aculeataare new records from Assam. Besides, we recorded the OrientalBrachionusdonneri(Fig.2e)andLecanesuperaculeata(Fig.2f), and the AustralasianNotommataspinata(Fig.2g) whileLecanedorysimilis(Fig.2h),L.hastata(Fig.2i),L.rhenana(Fig.2j) andMytilinamichelangellii(Fig.2k)are other interesting species.

Total rotifer richness in different beels ranged between 99 (Balaisuti)–124 (Sorbhog) species during the study period (Fig.3) with mean value of 110±10 species; it ranged between 65 (Baria) -92 (Sorbhog)and 82(Balaisuti) -108 (Sorbhog) species and recorded 67.8%–74.4% and 70.3%–78.4% community similarities (S?rensen’s index) amongst beels during two years, respectively. The monthly richness(Figs.4–7) ranged between 5–44 (23±11), 6–47(23±10), 4–56 (29±13) and 7–46 (27±9) species, and the rotifer community similarities ranged between 0–63.2% and 4.6%–71.0%; 0–85.7% and 8.2%–77.2%; 0–71.7% and 16.4%–54.5%; and 16.2%–69.8% and 32.7%–68.9% in Fingua, Baria, Sorbhog and Balaisuti beels during two years, respectively.Annual hierarchical cluster analysis of Rotifera amongst beels is presented in Figs.8–9. ANOVA registered significant richness variations amongst four beels (F3,69=3.382,P=0.023 0) and significant monthly variations (F3,23=4.627,P=3.902E-07)between them. Further, it registered significant annual richness variations in Baria (F1,11=7.604,P=0.018 6),Sorbhog (F1,11=5.167,P=0.037 1) and Balaisuti (F1,11=6.034,P=0.031 9) beels.

Fig.2 a. Cephalodella trigona (Rousselet ) (lateral view); b. Lecane bifastigata Hauer (dorsal view); c. Trichocerca hollaerti De Smet (lateral view); d. Trichocerca maior Hauer (lateral view); e. Brachionus donneri Brehm (ventral view); f. Lecane superaculeata Sanoamuang & Segers (ventral view); g. Notommata spinata Koste & Shiel (ventral view); h. Fig.19,Lecane dorysimilis Trinh Dang, Segers & Sanoamuang (dorsal view); i. L. rhenana Hauer (ventral view); j. Lecane hastata (Murray (ventral view); k. Mytilina michelangellii Reid & Turner (lateral view)

Lecanidae, Brachionidae, Lepadellidae and Trichocercidae indicated 46, 28, 22 and 15 species,respectively. Testudinellidae (9 species),Notommatidae (7 species), Euchlanidae (6 species)and Mytilinidae (6 species) are other species-rich families.Lecane(46 species),Brachionus(18 species),Lepadella(17 species) andTrichocerca(15 species) are important genera.Lecane/Brachionus(L/B) quotient indicated oscillating monthly variations(Fig.11) with mean values of 3.7±3.3, 3.5±4.1,4.1±5.1 and 4.5±2.7 in four beels, respectively.Sláde?ek’sBrachionus/Trichocerca(B/T) quotient followed oscillating monthly variations in all beels(Fig.10) with mean values of 1.6±1.5, 2.8±2.2,2.8±2.1 and 2.2±1.3 in Fingua, Baria, Sorbhog and Balaisuti beels, respectively.Of ten abiotic factors,only total alkalinity recorded significant negative correlation with richness (R=-0.597,P=0.002 1) in Balaisuti beel. The canonical correspondence analysis(CCA) co-ordination biplots of Rotifera richness with ten abiotic parameters (Figs.12–15) indicated cumulative influences of 88.15%, 80.72%, 94.70%and 92.04%, along two axes, in Fingua, Baria,Sorbhog and Balaisuti beels, respectively.

Fig.3 Species richness of Rotifera of Barpeta beels

4 DISCUSSION

We characterize Barpeta beels into two categories based on pH, specific conductivity, total alkalinity,total hardness and Calcium. Fingua and Sorbhog belonged to first category with circumneutral to slightly alkaline and moderately hard waters with low specific conductivity and calcium. Baria and Balaisuti beels with alkaline, hard and calcium rich waters with more than 2.5 times specific conductivity are grouped together. The second group differed from earlier reports on floodplains of Assam (Sharma and Sharma,2008, 2014a; Sharma, 2014, 2016; Sharma et al.,2015) and Manipur (Sharma, 2009a, 2009b, 2011;Sharma et al., 2016) states of NEI.

Fig.4 Monthly variations of Rotifera richness in Fingua beel (2011–2013)

Fig.5 Monthly variations of Rotifera richness in Baria beel (2011–2013)

Fig.6 Monthly variations of Rotifera richness in Sorbhog beel (2011–2013)

Fig.7 Monthly variations of Rotifera richness in Balaisuti beel (2011–2013)

Fig.8 The hierarchical cluster analysis of Rotifera assemblages (2011–2012)

Fig.9 The hierarchical cluster analysis of Rotifera assemblages (2012–2013)

Fig.10 Monthly variations of Brachionus / Trichocerca species ratios in beels (2011–2013)

Fig.11 Monthly variations of Lecane / Brachionus species ratios in beels (2011–2013)

A total of 160 rotifer species (S) observed from four beels is one of the richest assemblages of the taxon known from the Indian floodplains. This report is of biodiversity value as ～38.0% and ～57.0% of species known till date from India and NEI,respectively (BKS, unpublished). The biodiverse Rotifera is hypothesized to habitat diversity and environmental heterogeneity of the sampled wetlands.Our results supported hypothesis of Segers et al.(1993) indicating (sub) tropical floodplains to be the world’s rotifer rich habitats. The diverse nature corroborated with the results from the floodplains of Argentina (de Paggi, 1993, 2001), Brazil (Bonecker et al., 1998) and Australia (Shiel et al., 1998). Further,35 genera and 19 families recorded presently affirmed higher diversity of the taxon.

Fig.12 CCA coordination biplot of Rotifera richness and abiotic factors of Fingua beel

Fig.13 CCA coordination biplot of Rotifera richness and abiotic factors of Baria beel

Cephalodellatrigonais new to the Oriental Rotifera. The present report of this palaearctic species(Segers, 2007) extended its distribution to the Indian sub-region.Lecanebifastigatais new to NEI. This lecanid is known from Palaearctic and Oriental regions (Segers, 2007) and it is validly reported from India from West Bengal (Sharma, 1979; Sharma and Sharma, 2014c).Trichocercahollaerti,T.maiorandDissotrochaaculeataare new records from Assam.The first two species are added to the Indian Rotifera from Mizoram (Sharma and Sharma, 2015b) and are also reported from Loktak Lake (a Ramsar site),Manipur (Sharma et al., 2016) whileD.aculeatais reported from India from a wetland of Meghalaya(Sharma, 2016). Besides, our earlier report (Sharma and Khan, 2016) from these beels addedTestudinella dendradenaandBrachionusbenninias new to the Indian Rotifera and to the rotifer fauna of Assam,respectively.

Fig.14 CCA coordination biplot of Rotifera richness and abiotic factors of Sorbhog beel

Fig.15 CCA coordination biplot of Rotifera richness and abiotic factors of Balaisuti beel

Twenty-three globally interesting species formed an important fraction (14.4% of S) of biogeographic value. These included (i) the AustralasianBrachionus dichotomusreductus,B.kosteiandNotommata spinata; (ii) the Oriental endemics:Brachionus donneri,Keratellaedmondsoni,Lecaneblachei,L.bulladiabolica,L.niwati,L.superaculeataandFiliniacamasecla; (iii) the paleotropical species namelyKeratellajavana,Lepadelladiscoidea,L.vandenbrandei,Lecanelateralis,L.simonneae,L.unguitata,Testudinellabrevicaudata,T.greeniandTrichocercahollaerti; the palaeotropicalCephalodella trigona; HolarcticTrichocercamaior; the Indo-ChineseLecanedorysimilisand the cosmo(sub)tropicalBrachionusdurgae. Of these, comments on 15 species are made earlier by Sharma and Khan(2016).

Brachionusdiversicornis,B.forficula,Keratella javana,Lecanelateralis,L.simonneae,L.unguitata,Lepadelladiscoidea,L.vandenbrandei,Testudinella brevicaudataandT.greeniare ‘Eastern hemisphere elements’ (vide Segers, 2001).Brachionusdichotomus reductus,B.kostei,Keratellajavana,Lepadella benjamini,L.vandenbrandei,Lecanebifastigata,L.blachei,L.dorysimilis,L.niwati,L.rhenana,L.rhytida,L.superaculeata,Monommatagrandis,Notommataspinata,Testudinellaamphora,T.brevicaudata,T.dendradena,T.greeni,T.tridentata,TrichocercabidensandT.hollaertiare species of regional value in the Indian sub-region with distribution restricted till date to NEI. In addition,Brachionusbennini,B.donneri,B.leydigii,Filinia camasecla,F.saltator,Keratellaedmondsoni,K.tecta,Lacinulariaflosculosa,Lecaneaspasia,L.bifurca,L.bulladiabolica,L.haliclysta,L.lateralis,L.pusilla,L.simonneae,L.undulata,Lepadella biloba,L.costatoides,L.dactyliseta,L.discoidea,L.quinquecostata,L.triba,Macrochaetuslongipes,Mytilinamichelangellii,Platyiasleloupi,Trichocerca insignis,T.maior,T.scipioandT.tigrisare species with restricted distribution in the Indian sub-continent.

The overall rotifer richness (S) is lower than 207,218 and 252 species known from the floodplains of Africa (Segers et al., 1993), South America (Bonecker et al., 1998) and Australia (Shiel et al., 1998),respectively. This comparison needed caution as our inventory included only planktonic and semiplanktonic taxa. Total richness compared well the report of 164 species from 15 beels of lower Assam(Sharma, 2005); 162 species from Loktak Lake,Manipur (Sharma et al., 2016). On the other hand,rotifera of lower Assam beels is diverse than the reports of 144 species from the Majuli floodplains,upper Assam (Sharma et al., 2015), 124 species from seven beels of lower Assam (Sharma and Sharma,2001) and 110 species (Arora and Mehra, 2003) from the backwaters of the river Yamuna at Delhi.

Our collections indicated diverse Lecanidae(28.7% ofS) and the collective importance (40.0% ofS) of Brachionidae ＞ Lepadellidae ＞ Trichocercidae.These four Eurotatoria families exhibited biodiversity interest (69.4% ofS) concurrent with the reports from Deepor beel (Sharma and Sharma, 2015a) and Loktak Lake (Sharma et al., 2016). The notable richness of Brachionidae (17.5% ofS) and ofBrachionusspp.(11.2%) concurred with the report from Deepor beel(Sharma and Sharma, 2015a) but it contrasted than brachionid paucity reports of Sharma (2009a, 2009b,2014) and Sharma et al. (2015, 2016) from NEI. High brachionid diversity in Barpeta beels is attributed to their alkaline hard waters and to limnetic conditions created due to mass removal of aquatic vegetation during fishing. The species of littoral-periphyticLecane＞ Lepadella ＞Trichocerca, together,comprised a notable fraction (～49.0% ofS). The stated importance supported hypothesis of Green(2003) on the possibility of assemblage rules for the periphytic community. Further, this salient feature concurred with the reports from the floodplains of Brazil (Segers et al., 1993; Segers and Dumont,1995), Thailand (Sanoamuang 1998), Bolivia (Segers et al., 1998) and South Africa (Green, 2003) and India(Sharma and Sharma, 2014a). The rich nature and common occurrence of ‘tropic-centered genera’LecaneandBrachionus, more cosmopolitan species(～63.0% ofS), and collective richness (～20% ofS) of cosmotropical and pantropical species imparted‘tropical character’ to Barpeta Rotifera. This generalization is concurrent with composition of several tropical rotifer faunas (Green, 1972; Fernando,1980; Dussart et al., 1984; Segers, 1996, 2001).

We observed high overall rotifer richness in four beels (99–124, 110±10 species) with Sorbhog ＞Fingua ＞ Baria ＞ Balaisuti beels. The mean richness concurred with the reports of 114 species (de Paggi,2001) from the Rio Pilcomayo National park (a Ramsar site), Argentina; 106 taxa from Thale-Noi Lake, Thailand (Segers and Pholpunthin, 1997); and 104 species from Laguana Bufeos, Bolivia (Segers et al., 1998). Rotifera of Barpeta beels is, however, more biodiverse than the previous report of 73 species from Fingua beel (Sharma, 2005) and from the reports of 85 species (Sharma and Sharma, 2012), 69–93 species(Sharma and Sharma, 2008) and 60–100 species(Sharma et al., 2015) from various beels of Assam.Our report also showed diverse nature than the records of 71 and 75 species from Utra and Waithou pats(Sharma, 2011) and 62–73 species from 15 pats of Manipur (Sharma, 2009b). Total richness indicated inter-annual variations with higher range and mean during second year. High community similarities(67.8%–74.4% and 70.3%–78.4%) noticed during two years, respectively reflected homogeneity in the rotifer species composition amongst beels. This generalization is also supported by occurrence of 41 species (25.6 % of S) in all beels. ANOVA registered significant richness variations amongst four beels and significant monthly variations between them. The hierarchical cluster indicated the rotifer affinity between Fingua and Baria beels while Sorbhog beel showed distinct divergence during both years.

Individual beels are characterized by heterogeneity in Rotifera composition as endorsed by wider monthly richness variations, lower mean values, and lower yet wider community similarities in majority of instances and lack of occurrence of any species throughout the study period in any beel. The rotifer heterogeneity in individual beels is hypothesized to habitat disturbance due to fishing and removal of weeds though specific observations are desired this with effect. ANOVA registered significant annual richness variations in Baria, Sorbhog and Balaisuti beels.

Lecane/Brachionus(L/B) quotient mean values affirmed general littoral-periphytic character of different beels but oscillating monthly variations yet depicted habitat changes. The latter is reflected by low L/B values during January–April and February–June in Fingua; December–March, August–February and May–June in Baria; December–April, July–August, November and March–May in Sorbhog; and January, October and December in Balaisuti beel during the study period. Nevertheless, L/B values ＞6.0 and ＞ 10.0, observed during certain months and indicating typical wetland character in all beels, are attributed to lowBrachionusrichness or lack of species of the genus, respectively. The results, though not indicative of definitive patterns, asserted usefulness of L/B quotient vis-à-vis habitat changes in the sampled beels.

Brachionus/Trichocercaquotient (vide Sláde?ek,1983), an analogue of phytoplankton indices to establish trophic status of lentic or lotic waters,followed oscillating monthly variations in all beels while mean values indicated overall ‘mesotrophic’nature of four beels. Nevertheless, B/T recorded values up to 1.0 in 18, nine, seven and eight months in Fingua, Baria, Sorbhog and Balaisuti beels,respectively while ＞3.0 values are recorded in eight and nine instances in Baria and Sorbhog beels,respectively while Fingua and Balaisuti beels recorded‘eutrophic’ character in three and two instances,respectively. Sladecek’s quotient depicted trophic status variations in the sampled beels; the results ascertained reliability of use of this quotient under Indian conditions concurrent with the remarks of Sharma and Dudani (1992), and Sharma and Lyngskor(2003).

The lack of impact of individual abiotic factors on the rotifer richness in Barpeta beels is endorsed by only significant negative correlation of total alkalinity in Balaisuti beel. The canonical correspondence analysis affirmed higher cumulative influences(80.72%–94.70%) in different beels along two axes with higher values ＞92.0% in Sorbhog and Balaisuti beels. Chloride, rainfall and total harness; rainfall,water temperature, total hardness; water temperature,chloride, total alkalinity; water temperature, free carbon dioxide and calcium influenced richness of Rotifera in Fingua, Baria, Sorbhog and Balaisuti beels, respectively in CCA bi-plots.

5 CONCLUSION

The speciose and diverse Rotifer assemblage, taxa of global and regional distribution interest and Eastern Hemisphere species impart biodiversity importance to this study as well as value for meta-analysis of the rotifer diversity in the Indian floodplains. The richness variations amongst and within different beels vis-àvis homogeneity or heterogeneity in species composition, oscillating monthly richness, cumulative influence of abiotic factors rather than of individual factors, generalizations and variations of B/T and L/B quotients are useful attributes of ecosystem diversity.

6 ACKNOWLEDGEMENT

The senior author (BKS) thanks the Head,Department of Zoology, North-Eastern Hill University, Shillong for laboratory facilities. The samples analyzed for this study were collected by SIK. The authors have no conflict of research interests.Finally, we sincerely thank our anonymous reviewers for their valuable comments and suggestions.

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Sharma B K, Sharma S. 2015a. New records of rotifers(Rotifera: Eurotatoria) from Deepor beel—a Ramsar site of India with an update on its rich Rotifer diversity.JournalofThreatenedTaxa,7(3): 7 011-7 016.

Sharma B K, Sharma S. 2015b. Biodiversity of freshwater rotifers (Rotifera: Eurotatoria) of Mizoram, Northeast India: composition, new records and interesting features.InternationalJournalofAquaticBiology,3(5): 301-313.

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Sharma B K. 2009b. Rotifer communities of floodplain lakes of Manipur (North-East India): biodiversity, distribution and ecology.JournaloftheBombayNaturalHistory Society,106(1): 45-56.

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Sharma B K. 2016. Interesting rotifers (Rotifera: Eurotatoria)from a subtropical wetland of Meghalaya, Northeast India: new records.TurkishJournalofZoology,40(3):433-437.

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