Physics and Chemistry of the Earth 50–52 (2012) 140–148

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Physics and Chemistry of the Earth

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Mentum deformities in Chironomidae communities as indicatorsof anthropogenic impacts in Swartkops River

O.N. Odume ⇑, W.J. Muller, C.G. Palmer, F.O. ArimoroUnilever Centre for Environmental Water Quality, Institute for Water Research, Rhodes University, P.O. Box 94, Grahamstown, South Africa

a r t i c l e i n f o a b s t r a c t

Article history:Available online 24 August 2012

Keywords:ChironomidaeDeformitiesSouth AfricaSwartkops RiverWater quality

1474-7065/$ - see front matter � 2012 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.pce.2012.08.005

⇑ Corresponding author. Tel.: +27 730302687.E-mail address: nelskaro@yahoo.com (O.N. Odume

Swartkops River is located in Eastern Cape of South Africa and drains a heavily industrialised catchmentand has suffered deterioration in water quality due to pollution. Water quality impairment in the Swartk-ops River has impacted on its biota. Deformities in the mouth parts of larval Chironomidae, particularly ofthe mentum, represent sub-lethal effects of exposure to pollutants, and were therefore employed asindictors of pollution in the Swartkops River. Chironomid larvae were collected using the South AfricanScoring System version 5 (SASS5) protocol. A total of 4838 larvae, representing 26 taxa from four sam-pling sites during four seasons were screened for mentum deformities. The community incidences ofmentum deformity were consistently higher than 8% at Sites 2–4, indicating pollution stress in the river.Analysis of variance (ANOVA) conducted on arcsine transformed data revealed that the mean communityincidence of mentum deformity was significantly higher (p < 0.05) at Site 3. ANOVA did not reveal statis-tically significant differences (p > 0.05) between seasons across sites. Severe deformities were consis-tently higher at Site 3. Strong correlations were found between deformity indices and theconcentrations of dissolved oxygen (DO), total inorganic nitrogen (TIN), orthophosphate–phosphorus(PO4–P), electrical conductivity (EC) and turbidity.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Integrated water resources management (IWRM) requires aholistic approach to assess the impacts of water quality deteriora-tion on in-stream biota (NWRS, 2004). Such an approach would re-quire that effects of contaminants on aquatic ecosystems aredetected early enough in order to take appropriate mitigation mea-sures. Biological monitoring of rivers and streams is used to assessthe impacts of water quality deterioration on in-stream biota(Rosenberg and Resh, 1993; Bonada et al., 2006; Odume andMuller, 2011). Most biological water quality monitoring tools em-ployed in South Africa (e.g. the South African Scoring System ver-sion 5, Dickens and Graham, 2002) are based on communityresponses to water quality impairments. However, communitystructure assessments are essentially measures of lethality, andconcentrations of contaminants must be high enough to result inthe disappearance, or reduced abundances and diversities of sensi-tive taxa before community response approach would detect im-pacts of water quality stressors. Lethal end points are notsuitable for use as early warning indicators of water quality dete-rioration in freshwater systems (Faria et al., 2006). Therefore, thereis need for improved and holistic early warning biological water

ll rights reserved.

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quality monitoring tools, capable of detecting sub-lethal in-streameffects on biological communities. Morphological deformities inthe mouth parts of larval Chironomidae, particularly of the men-tum, represent sub-lethal response to in-stream pollutants andare therefore considered early warning indicators of water qualitydeterioration (Janssens de Bisthoven and Gerhardt, 2003; Nazarovaet al., 2004; Ochieng et al., 2008; Odume, 2011).

The term ‘‘deformity’’ refers to morphological features thatdepart from the normal Chironomidae larval configuration(Warwick, 1985; Nazarova et al., 2004; Ochieng et al., 2008), andeffects produced by mechanical wear, breakage or abrasion areusually not included in deformity screening, and are recognisedby their ‘‘chipped’’ or ‘‘rough’’ edges (Vermeulen, 1995; Bird,1997; Nazarova et al., 2004). Based on fossils records, the naturalincidences of chironomid deformities in unpolluted water bodieswere reported to range between 0% and 0.8% from the Bay ofQuinte, Canada (Warwick, 1980). However, because of increasedindustrialisation, urbanisation and agricultural activities, pristinewater bodies are scarce and numerous field studies (e.g. Warwick,1988; Nazarova et al., 2004; Ochieng et al., 2008) have reportedbackground levels of deformities in least impacted sites to rangebetween 0% and 8%, above which a site could be consideredcontaminated. Expressions of morphological deformities in larvalChironomidae inhabiting variety of aquatic environment have beenused as indicators of pollution arising from different pollutants

O.N. Odume et al. / Physics and Chemistry of the Earth 50–52 (2012) 140–148 141

such as heavy metals (Diggins and Stewart, 1998; Jeyasingham andLing, 2000; Martinez et al., 2002; Ochieng et al., 2008), acid minedrainage (Janssens de Bisthoven et al., 2005) and organic contam-inants (Servia et al., 1998, 2000; MacDonald and Taylor, 2006).Therefore, assessment and quantification of morphological defor-mities in larval Chironomidae offer an effective and cost friendlymeans of investigating impacts of environmental stressors onaquatic ecosystems (Meregalli et al., 2002). Although several struc-tures including the mentum, mandible, ligula, paraligula, pectenepipheryngis and antennae in Chironomidae larvae have beenexamined for deformities in other studies (Warwick, 1985; Jans-sens de Bisthoven and Gerhardt, 2003; Bhattacharyay et al.,2005; Veroli et al., 2008), only the mentum was chosen for thisstudy because it has proven to be the most useful structure as itappears to have a wider response range, easy to prepare for exam-ination and deformities quantified rapidly (Odume, 2011).

The Swartkops River located in Eastern Cape of South Africa is animportant ecological asset that supports an estuary that providesimportant breeding habitats for water birds and fish, and also servesas a recreational field (Taljaard et al., 1998). However, the increasinghuman activities in the catchment have resulted in the discharge ofpollutants into the river, which have negatively impacted on its bio-ta (Odume, 2011; Odume and Muller, 2011). Consequently, morpho-logical deformities in the mentum of Chironomidae communitieswere applied as a tool to evaluate sub-lethal effects of pollution onthe Swartkops River biological benthic community. Although Chiro-nomidae larval deformities have been successfully used in otherparts of the world as a biomonitoring tool, its potential as an indica-tor of pollution stress in South African fresh water resources has notbeen explored. The aims of this study therefore were to: documentand illustrate deformities in mentum of larval of different generaor species of Chironomidae; compare incidences of mentum defor-mities between genera/species of Chironomidae; evaluate seasonalvariations in the incidences of mentum deformities; and contributebaseline information for using Chironomidae mentum deformitiesas a biomonitoring tool in South African freshwater resources.

2. Materials and methods

2.1. Study area description and sampling sites

Swartkops River is located in Eastern Cape of South Africa anddrains a catchment of about 1555 km2, and has its origin in theGroot Winterhoek Mountains (DWAF, 1996; Odume, 2011). Theriver arises from the confluence of the Kwazunga River to the northand the Elands River to the southwest. Both the Kwazunga andElands Rivers originate in the Groot Winterhoek Mountains andjoin just above Uitenhage in an area called Kruisrivier to formthe Swartkops River, which discharges into the India Ocean atAlgoa Bay in Port Elizabeth (Fig. 1).

Although the upper catchment of the Swartkops River lies with-in a pristine inaccessible area of the Groot Winterhoek Mountains,the lower catchment is subjected to different sources of pollutionincluding discharges from wastewater treatment works, effluentsfrom tannery, wool processing factories as well as run-off frominformal settlements and storm water canals (Taljaard et al.,1998; DWAF, 1996; Bornman and Klages, 2005). These combinedsources of pollution contribute to the overall poor water qualitystatus, and reported elevated heavy metal concentrations in theriver (Binning and Baird, 2001; Odume, 2011; Odume and Muller,2011).

Climate in the catchment is generally temperate and warm, butreceives rain throughout the year with a minimum monthly aver-age of 60 mm (Nelson Mandela Bay Municipality, 2006). The geol-ogy of the catchment consists of cretaceous shale of mudstones

overlain by marine sedimentary deposits in the high lying regionsand by various alluvial deposits on the floodplain (Fromme, 1988).

The study was undertaken in four seasons at four sampling sites(Sites 1–4) over a period of 1 year. Site 1 (S33�45008.400E25�200

32.600) is located upstream of Uitenhage and represents least im-pacted conditions (reference site) within the accessible areas ofthe river. It was selected in agreement with criteria by Reynoldsonet al. (1997) and based on an expert judgment taking into consid-eration the quality and quantity of macroinvertebrate habitats, ex-tent of human impacts as well as accessibility. Site 2 (S33�47029.000

E25�24026.400) is located in the industrial city of Uitenhage and isimpacted by run-off from surrounding informal settlements, andby agricultural activities including livestock farming. Site 3(S33�47011.800E25�27058.7) is located further downstream of theindustrial city of Uitenhage. The site is impacted by industrialand wastewater effluents as well as by agricultural activities suchas live stock farming and crop cultivation. The wastewater effluentinput at this site has resulted in elevated nutrient levels leadingto extensive growth of aquatic weeds. Site 4 (S33�47034.000

E25�27058.700) is located at despatch close to a sand mining area,and is impacted with agricultural and municipal runoff, whichhave consequently resulted in a thick growth of aquatic weedsand discoloured water. A fifth site further downstream could notbe selected for system self recovery monitoring because the tidalmark at Perseverance is a short distance downstream of Site 4(Fig. 1).

2.2. Physicochemical variables

Water chemistry variables were measured once per season forfour seasons at the four sampling sites over the study period. Onsite, mid-channel dissolved oxygen (DO), electrical conductivity(EC), turbidity, temperature and pH were measured using Cyber-scan DO 300, Cyberscan Con 300, Orbeco-Hellige 966, mercury-in-glass thermometer and Cyberscan pH 300 metres respectively.Water samples collected in acid washed bottles were transportedto the laboratory, preserved at 4 �C, and analysed within 24 h for5-day biochemical oxygen demand (BOD5), orthophosphate–phos-phorus (PO4–P), nitrite–nitrogen (NO2–N), nitrate–nitrogen (NO3–N),ammonium–nitrogen (NH4–N) and total inorganic nitrogen.Five-day biochemical oxygen demand (BOD5) was analysedaccording to APHA (1992), while NO3–N and NO2–N were analysedaccording to Velghe and Claeys (1983), and APHA (1971) respec-tively. Spectroquant� phosphate and ammonium concentrationtest kits were used to analysed for orthophosphate–phosphorusand ammonium–nitrogen according to manufacturer’s instruc-tions. Palmer et al. (2005) method was adopted for the calculationof total inorganic nitrogen (TIN).

2.3. Chironomid sampling and screening head capsule for mentumdeformities

Concurrent with physicochemical sampling, Chironomidae lar-vae were sampled at the four sampling sites in accordance withthe SASS5 protocol (Dickens and Graham, 2002). Chironomid larvaewere collected from three distinct biotopes, namely: stones (stonesin- and out- of current), vegetation (marginal and aquatic vegeta-tion) and sediment (gravel, sand and mud). Chironomidae larvaewere preserved in 70 % ethanol and transported to the laboratoryfor sorting, identification, abundance counts and deformity screen-ing. Sorted chironomids were kept in specimen vials containing70% ethanol to prevent the head capsule from becoming dry as driedand shrunken head capsules are difficult to mount (Dickman andRygiel, 1996). The head capsules were mounted for taxonomicidentification using mouth parts and other structures according tothe keys described by Wiederholm (1983), Cranston (1996) and

Fig. 1. Map of Swartkops River showing sampling sites, urban areas and waste water treatment woks.

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Harrison (2002). The mounting procedures of Ochieng et al. (2008)were followed but cold potassium hydroxide (KOH) was used as aclearing agent instead of hot KOH (Warwick, 1988). Cold KOH as aclearing agent was found to produce better results than warmKOH. Mounted specimens were screened for mentum deformitiesunder an Olympus compound microscope (B � 51) equipped withan Altra 20 soft imaging system digital camera. For the subfamilyTanypodinae, the ligula was screened instead of the mentum be-cause the mentum is reduced and obscure in this subfamily. Alllarvae with broken or ambiguous deformities were considered asnormal specimens and only clearly deformity types derived from acombination of Lenat (1993), Janssens de Bisthoven et al. (1998),Martinez et al. (2002, 2003, 2006), Bhattacharyay et al. (2006) andOchieng et al. (2008) were identified as deformed specimens. Sepa-rated body segments were mounted separately and used duringidentification of specimens. Depending on the specimen’s size, amagnification of 10� or 40� was used and all image analysisand photos were taken using the software analySIS Five softimaging system.

2.4. Data analysis

Physicochemical variables were compared using one-way anal-ysis of variance (p < 0.05). Community incidences of mentumdeformities were calculated as the percentage of the number ofall deformed larvae irrespective of genera to the total larvae sam-pled for each site per season (Janssens de Bisthoven and Gerhardt,2003; Ochieng et al., 2008). Community incidences of deformitieswere arcsine transformed and ANOVA was used to compare differ-ences between sites, and seasons. The deformity incidences (DI)calculated as the percentage (i.e. proportion) of deformed individ-uals to the total number of larvae screened within a taxon in se-lected Chironomidae taxa taken from the same site (i.e. exposedto the same environmental conditions over time) were compared.Taxa were selected for this analysis if there were at least 20 larvaewithin a site and also occurred in more than one sampling season.Such criteria were necessary because deformity incidences (i.e.proportion of deformed individuals) are highly dependent on sam-ple size and a very small sample size could result in unrealisticallyelevated incidence of deformity. To facilitate the comparison of

mean percentage deformity incidence, it was also important thatselected taxa occurred in more than one sampling season to avoidseasonal bias. However, it was also pertinent not to set inappropri-ately stringent criteria, considering the low abundances of most ofthe chironomid taxa recorded at the four sites during the foursampling seasons. A sample size of at least 20 larvae per taxonhas been reported in literature for comparison (MacDonald andTaylor, 2006) and was considered appropriate in this study. ANOVAwas conducted using the Statistica software package version 9.

Redundancy Analysis (RDA) was used to investigate the correla-tions between physicochemical variables and community inci-dences of deformity (CID), Orthocladiinae deformity incidences(DI-Orth), Tanypodinae deformity incidences (DI-Tany), Chirono-mini deformity incidences (DI-Chi) and Tanytarsini deformity inci-dences (DI-Ttar). For the RDA, pH and BOD5 were excluded fromthe analysis because they showed high multi-colinearity (R > 0.8).A Monte-Carlo permutation test with 100 permutations wasapplied to test the significance of the model. RDA was undertakenusing the computer programme Environment Community Analysis1.33 Package (ECOM) (Pisces Conservation Ltd., 2000).

3. Results

3.1. Physicochemical data

Physicochemical results are provided in Table 1.

3.2. Screening Chironomidae communities for larval morphologicaldeformities

A total of 4838 chironomid larvae from the four samplingsites during the four sampling seasons were screened for deformi-ties in the mentum and ligula. Individuals of the tribe Chironominiwere more deformed compared to members of other subfamiliesand tribe Tanytarsini (Table 2). The community incidences ofmentum deformity were consistently highest at Site 3 throughoutthe sampling seasons and were higher than 8% at Sites 2–4, indicat-ing pollution stress in the Swartkops River (Fig. 2). Analysis ofvariance (ANOVA) conducted on arcsine transformed data revealedthat the mean community incidence of mentum deformity was

Table 1Physicochemical characteristics, mean ± standard deviation, and ranges (in parenthesis) of the four sampling sites in the Swartkops River during the sampling seasons. Numbersin parenthesis are ranges and (n = 4).

Variable Site 1 Site 2 Site 3 Site 4 P-value

Dissolved oxygen (mg/l) 6.07 ± 1.13 (4.73–7.48) 6.99 ± 1.84 (5.53–9.48) 3.26 ± 0.54 (2.63–3.89) 2.17 ± 1.3 (0.9–3.79) 0.001pH 6.61 ± 1.17 (5.13–7.75) 7.12 ± 1.08 (5.69–8.25) 7.36 ± 0.42 (6.97–7.9) 7.27 ± 0.56 (6.65–8.01)Temperature (�C) 17.88 ± 4.44 (12.5–22.0) 17.71 ± 7.72 (9.8–27.3) 20.13 ± 4.49 (14.3–25.2) 18.55 ± 5.43 (12.2–24.0)Electrical conductivity (mS/m) 32.58 ± 4.69 (28.1–39.0) 407.5 ± 84.5 (300–488) 212.78 ± 79.9 (154.8–331) 268.5 ± 37.6 (234–322) 0.000Turbidity (NTU) 8.75 ± 7.89 (3.68–10.1) 6.15 ± 1.47 (4.7–8.0) 115.63 ± 139.2 (10.5–320) 9.35 ± 11.22 (2.2–26) 0.012BOD5 (mg/l) 4.21 ± 1.96 (2.16–6.86) 8.66 ± 5.47 (4.78–16.68) 14.66 ± 5.15 (8.32–20.62) 13.58 ± 6.85 (7.06–22.94) 0.012Total inorganic nitrogen (TIN) (mg/l) 0.171 ± 0.22 (0.039–0.49) 1.567 ± 2.26 (0.169–4.92) 7.2 ± 2.51 (5.19–10.84) 6.34 ± 3.62 (1.59–10.19) 0.001Orthophosphate phosphorus (PO4–P)

(mg/l)0.013a 1.11 ± 0.56 (0.463–1.5) 7.46 ± 4.05 (2.17–11.98) 7.59 ± 1.35 (6.86–9.61) 0.001

a Indicates variables detected once. P-values are shown for variables that were significantly different (P < 0.05).

Table 2Incidences of mentum and ligula deformities among chironomid subfamilies/tribes sampled at the four sites during the four sampling seasons. Numbers in parentheses arepercentage deformed while numbers outside of parenthesis are actual numbers of larvae sampled.

Subfamily/tribe Site

Site 1 Site 2

Spring Summer Autumn Winter Spring Summer Autumn Winter

Orthocladiinae 222 (4.5) 120 (5) 103 (6.8) 54 (1.9) 300 (9.7) 39 (2.6) 1Chironomini 48 (14.5) 2 9 7 29 (17.2) 443 (9.7) 196 (10.8) 28 (10.7)Tanytarsini 16 (6.3) 15 21 (4.8) 60 (5) 12Tanypodinae 20 11 (9.1) 10 1 221 (7.7) 26

Site 3 Site 4

Orthocladiinae 5 10 (10) 6Chironomini 540 (21.6) 647 (21.8) 472 (15.5) 517 (13.7) 31 (19.4) 129 (16.7) 24 (12.5) 429 (9.9)Tanytarsini 1 4 (25) 9Tanypodinae

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significantly higher (p < 0.05) at Site 3. ANOVA did not revealstatistically significant differences (p > 0.05) between seasonsacross sites.

3.3. Spatial and temporal patterns of mentum deformities inChironomidae larvae

The patterns of mentum and ligula deformities among chirono-mid taxa at the four sampling sites during the four sampling sea-sons are presented in Fig. 3 and illustrated in Figs. 4a and 4b. AtSite 1, missing teeth and fused teeth were the commonest typesof deformities during the four sampling seasons. Although splitteeth were observed among chironomid taxa at this site, they wereless common throughout the sampling seasons than other types ofdeformities. At Site 2, during spring, fused teeth, Köhn gaps and

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Fig. 2. Percentage Chironomidae larval community incidences of mentum defor-mities at each of the four sampling sites in the Swartkops River during the foursampling seasons. Numbers above each column are sample sizes.

missing teeth were the commonest types of deformities whilemissing teeth was the most dominant type of deformity observedamong chironomid taxa during summer and autumn. However,in autumn, multiple deformities (i.e. a single larvae showing morethan one type of deformity in the mentum) were observed. Duringwinter, only fused teeth were recorded at this site and althoughdeformity types such as extra teeth, asymmetry and split teethwere observed in other sampling seasons, they were less frequent(Fig. 3).

At Site 3, chironomid taxa were characterised by Köhn gap,asymmetry, fused, missing, split, and extra teeth during the foursampling seasons. However, during winter and autumn, multipledeformities were observed among chironomid taxa at this site.Generally, more deformities were seen among individuals fromthis site compared to the other three sites. At Site 4, during spring,chironomid taxa were characterised by fused and extra teeth. Insummer, missing teeth and Köhn gaps were the dominant typesof deformities seen among chironomid taxa, while fused teethwere the only type of deformity seen during autumn. Chironomidtaxa at Site 4 during winter were characterised by missing teethand multiple deformities (Fig. 3).

3.4. Incidences of mentum deformities in selected Chironomidae taxaat the four sampling sites

At Site 1, incidences of mentum deformities between Cricotopussp.1, Cricotopus trifasciata gr. and Tanytarsus sp. were compared(Fig. 5). Mean incidence of mentum deformity was highest in C. tri-fasciata gr. but lowest in Cricotopus sp.1. At Site 2, incidences ofmentum deformities were compared between Cricotopus sp.1, C. tri-fasciata gr., Dicrotendipes sp. and Tanypus sp. Incidences of deformi-ties were highest in Dicrotendipes sp. but lowest in C. trifasciata gr(Fig. 5). At Site 3, incidences of mentum were compared betweenChironomus sp.1 and Chironomus sp.2. Incidences of deformities

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missing teeth

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Asymmetry

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multiple deformities

Fig. 3. Percentage occurrence of deformity types recorded in the mentum of chironomid taxa at each of the four sampling sites in the Swartkops River during the foursampling seasons.

Fig. 4a. Normal and deformed menta of Chironomidae. (a) Normal mentum of Chironomus sp.1. (b) Normal mentum of Chironomus sp.2. (c) Split median teeth of Chironomussp.1. (d) Missing left median tooth of Chironomus sp.1. (e) Kohn gap in Chironomus sp.1 (f) Fused median teeth of Chironomus sp.1. (g) Extra right median teeth in Chironomussp.2. (h) Fused median, third and fourth lateral teeth in Chironomus sp.1.

144 O.N. Odume et al. / Physics and Chemistry of the Earth 50–52 (2012) 140–148

Fig. 4b. Normal and deformed menta of Chironomidae. (h) Missing median tooth of Chironpmus sp.1. (i) Missing second left lateral tooth of Chironomus sp.1. (j) Normalmentum of Cricotopus sp.1. (k) Missing 3rd right lateral tooth of Cricotopus sp.1. (l) Kohn gap in mentum of Cricotopus sp.1. (m) Split 3rd right lateral tooth of Cricotopus sp.1.(n) Normal mentum of Tanytarsus sp. (o) Missing 5th right lateral tooth of Tanytarsus sp.

O.N. Odume et al. / Physics and Chemistry of the Earth 50–52 (2012) 140–148 145

were highest in Chironomus sp.1 (Fig. 5). No comparison was madeamong chironomid taxa at Site 4 because Chironomus sp.1 was theonly dominant taxa that occurred in more than one season at thissite. Results revealed that incidences of mentum deformities variedamong chironomid taxa taken from the same sites. However, one-way analysis of variance (ANOVA) conducted on arcsine trans-formed data revealed no statistically significant differences(p < 0.05) for the mean incidences of mentum deformities betweenchironomid taxa sampled at the same site.

3.5. Chironomidae larval mentum deformities and water chemistrycorrelations

Correlations between physicochemical variables and commu-nity incidences of deformity (CID), Orthocladiinae deformity inci-dences (DI-Orth), Tanypodinae deformity incidences (DI-Tany),Chironomini deformity incidences (DI-Chi) and Tanytarsini defor-mity incidences (DI-Ttar) were elucidated using RDA (Fig. 6). Onboth axes, TIN was positively correlated with all the deformity

Cri sp.1 Cri tri Dicro Tanypus

Mentum of selected chironomidspecies at site 2

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Fig. 5. Mean and standard deviation for percentage incidences of mentum deformities in in selected Chironomidae taxa at Sites 1–3. Abbreviations: Small squares = means,range bars = standard deviations, Cri sp.1 = Cricotopus sp.1 and Cri tri = Cricotopus trifasciata gr., Dicro = Dicrotendipes sp. Chir sp.1 = Chironomus sp.1 and Chir sp.2 = Chironomussp.2.

Axis 1210-1-2

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DI-orthDI-TtarDI-Tany CID DI-Chi

DO

Temp.

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TurbudityPO4-P

EC

Fig. 6. First two axes of RDA showing correlations between physicochemical variables and deformity incidences. Abbreviations: CID = community incidences of deformity,DI – Chi, DI – Orth, DI – Tany and DI–Ttar stand for deformity incidences for Chironomini, Orthocladiinae and Tanypodinae and Tanytarsini.

146 O.N. Odume et al. / Physics and Chemistry of the Earth 50–52 (2012) 140–148

indices (i.e. CID, DI-Orth, DI-Tany, DI-Chi and DI-Ttar). However,turbidity, EC and PO4–P exerted the highest influences on defor-mity indices.

4. Discussion

The elevated levels of community incidences of mentum defor-mities at Sites 2–4 in this study are indicators of pollution stressand possibly of heavy metals contamination, which have been re-ported from the Swartkops River in an earlier study (Binning andBaird, 2001). The observed low incidences of deformities at Site 1could be considered early indicators of water quality deterioration.Several studies (e.g. Diggins and Stewart, 1998; Martinez et al.,2002; Bhattacharyay et al., 2006) have implicated heavy metalsas causal agents of chironomid deformities. However, under fieldconditions, it is too simplistic to attribute observed incidences of

deformities to a single or group of chemical(s) because their inputsinto the natural environment not only encompass their pure statebut also their by-products as a result of degradation, synergisticand antagonistic interactions (Warwick, 1991; Hassan et al.,2005). As a result, in reality, organisms are exposed to a wide arrayof chemical contaminants in the aquatic environment. Therefore,the elevated mentum deformities observed at Sites 2–4 are indic-ative of biological effects of exposure to a wide array of pollutantsacting either synergistically, antagonistically, independently orpossibly even other environmental stressors, which may or maynot be linked to water quality. For example, Bird (1997) reportedthat substrates to which larvae are exposed influenced the levelsof deformities in chironomids. It will therefore be useful to inves-tigate whether factors not directly related to water quality such aspredation; habitat degradation and competition could also influ-ence deformities. Nevertheless, the strong correlations between

O.N. Odume et al. / Physics and Chemistry of the Earth 50–52 (2012) 140–148 147

incidences of mentum deformities and the concentrations of dis-solved oxygen (DO), orthophosphate-phosphorus (PO4–P), totalinorganic nitrogen (TIN), electrical conductivity, and turbidityseemed to suggest that organic inputs into the Swartkops Riverare also likely to induce deformities in chironomids. These defor-mities also reflect a biological community with unfit individuals.

Because deformities are important ecological endpoints of fit-ness, the ability of chironomid taxa to perform normal ecosystemfunctions such as recycling of nutrient could be impaired as a re-sult of effects on the feeding ability of chironomids with deformedmouth parts. Information on individual fitness in an ecosystem iscrucial in water resources management because a fit and healthycommunity depends on the fitness of the constituent individuals.Therefore, the elevated incidences of mentum deformities at Sites2–4 particularly at Site 3, indicate an ecosystem not functioningat an optimal level due to impaired individual species’ health.

Incidences of deformity varied among genera of chironomids re-ported in this study, with taxa within tribe Chironomini subfamilyChironominae expressing comparatively higher deformity inci-dences (Table 2). These taxa are mostly detrital feeders (Armitageet al., 1995) and their mouth parts are often in close contact withsediment bound contaminants, which may explain their elevateddeformity incidences. The relatively high incidences of deformityamong the Chironominae reported in this study are in agreementwith those reported by Bhattacharyay et al. (2006) and Ochienget al. (2008) who noted that incidences of deformities among generawithin this subfamily were comparatively higher than genera inother subfamilies. Incidences of deformities among the predaciousTanypodinae were relatively less frequent in the present study. Per-haps their feeding habits, being predators (Armitage et al., 1995), donot expose them so much to the sediment bound pollutants. Otherstudies have also noted low incidences of deformities among theTanypodinae: Bhattacharyay et al. (2006) for example reported few-er numbers of deformed Tanypodinae compared to Chironomini.

Differences in the expression of morphological deformitiesamong chironomid genera highlight the importance of screeningand tabulating deformities separately for each genus. Althoughthese differences were not statistically significant among dominantgenera taken from the same sites, they however suggest that theapplication of Chironomidae larvae deformities as a biologicalscreening tool requires independent reference or background val-ues for each genus. The different instar stages of larvae which werenot considered in this study may also influence the incidences ofdeformities observed among genera.

Several authors (e.g. Lenat, 1993; Bird, 1997; Al-Shami et al.,2011) who have used deformities in Chironomidae larvae as indi-cators of aquatic health have focused on the genus Chironomus.Although this genus is widely distributed and may be useful inassessing water quality impairments, it may not always be in suf-ficient numbers, especially at relatively clean sites. Therefore it re-mains important to screen deformities in other genera. Theoccurrence of deformities in other genera such as Tanytarsus sp.Cricotopus sp.1, C. trifasciata gr. and Tanypus sp. in the presentstudy highlights the importance of deformities screening in otherchironomid genera because each genus may have different refer-ence or background levels of sensitivity to pollutants. In addition,screening deformities in other chironomid genera allows for com-parison of sensitivity among genera in expressing morphologicaldeformities. Knowledge of differences in the expression of mor-phological deformities among chironomid genera could help indetermining sensitivity rating.

Although in Vermeulen’s (1995) review it was observed thatproportional occurrence of different deformity types shifted some-what consistently according to the type of prevailing pollution,there has not been any concerted effort to link different types ofdeformity to a particular contaminant and there appear to be some

degree of overlap among different deformities induced by differenttypes of contaminants (Janssens de Bisthoven et al., 2005;MacDonald and Taylor, 2006). However, it has been noted thatoccurrence of mentum gaps, or the so called Köhn gaps, arepredominantly characteristics of sites contaminated with heavymetals (Vermeulen, 1995; Groenendijk et al., 1998). Consequently,the occurrence of Köhn gaps at Sites 2–4 in this study is indicationof possible heavy metal contaminations at these sites, which havebeen reported in the Swartkops River in an earlier study (Binningand Baird, 2001). Furthermore, deformity types such as asymme-try, extra teeth and multiple deformities that characterised thementum of chironomid taxa at Sites 3 and 4, which were notobserved at Sites 1 and 2, suggest that these types of deformitieswere induced by severe pollution. Overall, the discriminatorycapacity of Chironomidae deformities as a biological screening toolcould be enhanced if deformity types and severity are linked todifferent types or concentrations of contaminants.

In order to account for possible seasonal variations, someauthors (e.g. Servia et al., 2000) have emphasised the importanceof screening deformities across seasons. However, in this study,no statistical significant differences were observed between sea-sons. The community incidences of mentum deformities were inmost cases higher during spring and summer at each of the foursampling sites (Fig. 2). Increased temperature during summer islikely to increase concentrations and bioavailability of contami-nants (Jeyasingham and Ling, 2000), and deformities are likely tobe elevated during this season. On the other hand, elevated inci-dences of deformities during spring has been attributed to spring‘‘overwintering’’ larvae that had been developing at a slower rateunder low temperature conditions and were therefore exposedmuch longer to contaminants (Jeyasingham and Ling, 2000). Con-trary to the observations of Servia et al. (2000) who reported high-er incidences of deformities during winter, in the present study, inmost cases, lower incidences of deformities were observed in win-ter and autumn (Fig. 2). However, during winter and autumn, morelarvae showed multiple deformities in a single individual, whichseemed to suggest more severe responses during these seasons(Fig. 3). Such severe responses are likely to be caused by prolongedexposure to pollutants as a result of slower rate of larval develop-ment under low temperature conditions.

In conclusion, screening of mentum deformities in Chironomi-dae provides evidence of sub-lethal effects of pollution on theSwartkops River chironomid communities and may serve as earlywarning indicators of deteriorating water quality. It also providesindication of species health and fitness of chironomids, whichcould impact on their ability to feed, and to perform ecologicalroles such as serving as a path-way for the transportation and util-isation of energy and matter in the Swartkops River. Furthermore,the elevated community incidences of mentum deformities re-corded at Sites 2–4 are indication of chemical stress in the Swartk-ops River while those recorded at reference site indicate responseto low concentrations of contaminants.

Acknowledgements

This research was funded by the Carnegie Corporation of NewYork through the Regional Initiative in Science and Education(RISE) programme. We are grateful to Dr Andrew Slaughter forassistance in the field, and the two anonymous reviewers for usefulcomments.

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