TOTAL SUSPENDED SOLIDS IN SURFACE WATERS VERSUS EMBRYONIC DEVELOPMENT OF PIKE (ESOX LUCIUS L.)

Małgorzata Bonisławska¹, Krzysztof Formicki², Izabela Smaruj³, Joanna Szulc^3
1 Department of Aquatic Sozology, West Pomeranian University of Technology in Szczecin, Szczecin, Poland
² Division of Hydrobiology, Ichthyology and Biotechnology of Biotechnology of Reproduction,
West Pomeranian University of Technology in Szczecin, Szczecin, Poland
³ Division of Hydrobiology, Ichthyology and Biotechnology of Biotechnology of Reproduction, West Pomeranian University of Technology in Szczecin, Szczecin, Poland

ABSTRACT

Effects of total suspended solids in riverine water on embryonic development and larval survival, size, and malformation rate in pike (Esox lucius L.) were studied. Total suspended solids in concentrations even below 25 mg · dm^-3 (the generally accepted threshold level) were found to inhibit fish embryogenesis by affecting fertilisation (% fertilisation: untreated, filtered riverine water and tap water: 75; 91; 85, respectively), perivitelline space formation (perivitelline space %: untreated, filtered riverine water and tap water: 29.77; 33.07; 29.68, respectively), organogenesis, and hatching (in riverine water – hatching began at 95 D° and terminated at 140 D°; in filtered riverine water – hatching began at 110 D° and terminated at 150 D°). The total suspended solids were also found to affect the larval size: the larvae hatched in water containing suspended 0particulates were smaller than those hatched in clean water (larvae hatched from eggs incubated in riverine water total length 9.34mm,  filtered water – 9.82 mm); the larval malformation rate was higher in the suspended solids-rich water (% malformed larvae – 9.0) than in clean water (% malformed larvae 7.0).

Key words: fish embryogenesis, pike, pike embryonic development.

INTRODUCTION

Particulates, both natural and originating from pollution, present in water are termed suspended solids. Natural suspended solids include autochthonous organic particulates produced by living organisms, resuspended bottom sediment, materials from eroded banks, and particulates brought in from the catchment. On the other hand, anthropogenic pollution is a source of undesirable particulates, some of them highly toxic [16,30].

Suspended solids are an environmental factor which may have a trophic importance; they may also scavenge and bind toxic substances. On the other hand, increased levels of suspended particulates may impinge on the quality of the habitat of living organisms, including fish. Increased turbidity caused by excessive levels of suspended particulates reduces penetration of light into the water column, which adversely affects photosynthesis. In addition, reduced amount of light in the water affects vision of aquatic organisms, including fish. In their study on salmonids kept in water of turbidity exceeding 2 NTU, Bash et al. [4] observed impaired feeding, which was translated later on the fish size. Adverse effects of high amounts of suspended particulates on salmonid spawning, growth, and reproduction were reported by Nogale [23], Berg [5], Lloyd et al. [20], Reid [25], and Soulsby et al. [29]. Increased levels of mineral particulates in the water may cause thickening of gill epithelium in the rainbow trout (Oncorhynchus mykiss (Walb.))[15].

High concentrations of suspended particulates affect both adult fish and embryos developing in eggs. Earlier studies on effects of short- or long-term exposure of various fish species to very high concentrations of suspended solids (300–175 thou. mg·dm^-3) involved juvenile or adult individuals [14,15,35]. Fish embryos, although isolated by the egg membrane from pollutants present in the water, are also exposed to suspended particulates, even when these occur at low concentrations. The Lake Balaton zander (Sander lucioperca (L.)) eggs showed increasing mortality when the concentration of suspended particulates increased as a result of heavy storms [24]. Schubel et al. [28], too, found adverse effects of increased concentration of natural particulates in water on the development and hatching success of the yellow perch (Perca flavescens Mitchell) and striped bass (Morone saxatilis Walb.). Particles sedimenting on the bottom, when settling on fish eggs, may adversely affect gas exchange by restricting oxygen availability to the embryo. This in effect may result in reduced hatching rate, as demonstrated by Kempińska [17] for the European whitefish (Coregonus lavaretus generosus (Peters)) and by Newcombe and Jensen [22] for the trout (Salmo trutta m. trutta L.).

Mineral particles suspended in water are less hazardous and easier to eliminate than organic suspensions, as it is only very seldom that they are accompanied by increased concentrations of nutrients (NH₄⁺; NO₂^-, NO₃^-). On the other hand, organic particulates (resulting from anthropogenic pollution) which may additionally cause bacterial and fungal infections, adversely affect fish egg development by directly or indirectly influencing the dissolved oxygen content in water. However, increased concentrations of mineral particulates may be accompanied by increased concentrations of ammonia nitrogen (NH₄⁺) and nitrates (NO₃^-); the oxygen regime may become impaired, causing the appearance of nitrites (NO₂^-) [19].

The water in fish spawning grounds, both natural and that in aquaculture should be devoid of suspended particulates which may impair oxygen conditions for the developing embryos even when the water itself is well-oxygenated. Increased concentrations of suspended particulates, caused by intensive fish culture, result in reduced production [13,30].

In the second half of the 20th century, an attempt was made to determine the maximum suspended particulates concentration that would be harmless for fish. Based on results of numerous studies, e.g., those of Buck [10], which served as a basis for reports published by EIFAC [11] and NAS [21], the suspended particulates concentrations lower than 25 mg dm^-3 were assumed to have no effect on fish production; the concentration range of 25–80 mgdm^-3 was assumed to maintain production at an acceptable level, while the range of 80–400 mg·dm^-3 was deemed unsuitable for fish farming. According to the Ministry of Environment Directive of 4 October 2002 on requirements to be met by inland waters which provide habitats for fish living under natural conditions [26], the annual mean total suspended solids concentrations, for both salmonids and cyprinids, should not exceed 25 mg·dm^-3. The Directive mentioned is a Polish regulation compatible with European Union's law regarding the quality of surface waters.

As shown by a review of the relevant literature, effects of suspended particulates on fish were addressed in numerous studies which focussed on adult individuals and on species sensitive to pollution, mainly salmonids.

This work was aimed at following effects of total suspended solids occurring naturally in riverine water on early developmental stages (embryogenesis) of the pike (Esox lucius L.). Determining the degree to which the embryonic development duration as well as larval survival and size are sensitive to suspended solids concentration may aid in understanding the effects of pollutants present in natural waters on fish development.

MATERIALS AND METHODS

The study was conducted in spring 2008 (March) and involved water collected from the downstream reaches of River Wiśniówka, situated in the catchment of River Ina which discharges into the Szczecin Lagoon in NW Poland (Treatments I and II). Treatment I involved water collected directly from the river; Treatment II involved the riverine water which was filtered through 40 mm diameter borosilicate filters (0.35 mm thickness; 0.3µm particle retention). The control (Treatment III) involved tap water.

Analyses of selected water quality parameters

Water in the three treatments was assayed before fertilization of the eggs – (as prescribed by appropriate Polish Standards, referred to in parentheses below), for the following water quality parameters:

• temperature and pH (PN-78/C-04578/04);

• total suspended solids (mg·dm^-3) (EN872: 2005);

• dissolved oxygen content (mgO₂·dm^-3) (PN-ISO5813);

• 5-day biochemical oxygen demand, BOD5 (mgO₂·dm^-3) (PN-EN 1899-1:2002);

• chemical oxygen demand, CODCr (mgO₂·dm^-3) (PN-ISO 6060:2006);

• conductivity, P (µS cm^-1) (PN-77/C-04542);

• total alkalinity (mgCaCO₃ dm^-3) (PN-90/C-04540/03);

• total hardness (mgCO₃ dm^-3) (PN-ISO 6059:1999);

• ammonia nitrogen concentration (mgN-NH₄⁺·dm^-3) (PN-76/C-04576/01);

• nitrate nitrogen concentration (III) (mgN-NO2·dm^-3) (PN-73/C-04576/06);

• total phosphorus concentration (mgP dm^-3) (PN-91/C-04537/09);

• total iron content (mg·dm^-3) (PN-ISO 6332:2001).

Egg incubation

The study material were the gametes (eggs: a mix of eggs from 3 females; sperm: a mix of sperm from 6 males) were obtained from adult pike caught in the River Regalica. The eggs were fertilized with the "dry" method  at an isothermal laboratory.

Fertilised pike eggs were placed in the basket containers and placed in the aerated aquaria with untreated riverine water (Treatment I), filtered riverine water (Treatment II), and tap water (Treatment III = control).

Water temperature during incubation was kept at 10.0 ± 0.5°C. Individual stages of the embryonic development were observed and recorded using an observation system consisting of a stereomicroscope (Nikon SMZ 1500) equipped with a microprocessor control (Trol–8100/9100), a digital camera (Nikon DS. Fi–1), a Nikon monitor, a VCR (JVC) recorded, and a computer [36]. The images recorded were used in the subsequent detailed analysis of the results.

Duration of the embryonic development was determined in degree-days (D°; a product of the number of days of embryogenesis and the mean daily temperature); the rate of embryogenesis was determined from the duration of individuals stages (in about 60% of the individuals examined): blastopore closure; eyeing (the presence of pigment in the eyes); and hatching, including its commencement, mid-point (50% eggs hatched), and termination During the embryonic development, the percentage of fertilised eggs was calculated (based on 50 eggs examined at the blastopore closure stage) as was the embryo survival rate (from the number of larvae hatched from the fertilised eggs picked out at the blastopore closure stage) and the percentage of malformed larvae.

Once the egg swelling was completed, the eggs were photographed and measured, using the Multiscan v. 13.01. software; two diameters were measured (± 0.001 mm) and averaged, following which the egg volume was calculated, as in [3]:

The hatched larvae (20 per treatment) were photographed and measured (total length or longitudo totalis, l.t.; yolk sac length, l, and height, h) (± 0.001 mm). The data were used to calculate the yolk sac volume (Ve) from the elongated ellipsoid volume formula [6]:

The results were processed using the Statistica 8.0 PL software (StatSoft Poland). The following statistical procedures were applied to test for significance of differences between the treatments: one-way analysis of variance (ANOVA, p = 0.01) for egg and oocyte size, yolk sac length and volume; Duncan's multiple range test (p = 0.05) to compare the sizes of eggs and oocytes and mean larval size parameters.

Egg membranes

On 35 Dº, 8 eggs were collected from each treatment and mounted for scanning electron microscope (SEM) examination of egg surfaces. The eggs were fixed with 4% formaldehyde, and dehydrated in the alcohol series (increasing concentration) and acetone. The dehydrated egg membranes were mounted on stubs and dusted with a gold-palladium alloy. The mounts were examined under an FEI Quanta 200 SEM and photographed.

RESULTS

Water quality analyses

The water quality analyses performed showed the water used in the treatments to differ in terms of levels of the quality indicators used (Table 1).

Table 1. Values of the water parameters (before fertilization of the eggs) selected for analyses: untreated riverine water (Treatment I), filtered water (Treatment II), and tap water (Treatment III) against threshold values set by the Ministry of Environment Directives of 4 October 2002 [26] and 20 August 2008 [27]

Parameter	Treatment			Threshold values set by Ministry of Environment directives of
				4 October 2002			20 August 2008
	I	II	III	fish			quality class
				salmonids		cyprinids	I	II
Temperature (°C)	10.5	10.5	10.5	<21.5 <10 *		<28.0 <10 *	≤22	24
pH	7.65	7.60	7.03	6.0-9.0			6-8.5	6.0–9.0
Suspended solid (mg·dm-3)	20	0	0	<25			≤25	50
Dissolved oxygen (mgO2dm-3)	10.96	11.04	10.55				≥7	5
Electrolytic conductivity. (µScm-1)	610	569	435	–			≤1000	1500
Alkalinity (mg CaCO3dm-3)	225	220	175	–			–
General hardness (mg CO3·dm-3)	225	217	215	–			–
Chlorides Cl-(mg·dm-3)	28.4	28.4	56.8	–			≤200	300
Ammonium nitrogen N-NH4+ (mg·dm-3)	0.047	0.038	0.009	<0.78			≤0.78	1.56
Nitrite nitrogen N-NO2– (mgN·dm-3)	0.045	0.040	0.005	<0.01	0.03		–
Total phosphorus (mgP·dm-3)	0.471	0.364	0.156	<0.2	0.4		≤0.2	0.4
Total iron  Fe2+3+ (mg·dm-3)	0.251	0.030	0.020	–			–

*the value applicable only for spawning periods and larval development of fish species which require cold water to breed and only to the water bodies capable of supporting such species

The concentration of total suspended solids were found to oscillate around 20 mg dm^-3, a level indicative of the water being suitable for fish egg incubation, according to the Polish regulations [26, 27]. The increased content of total suspended particulates in Treatment I (riverine water) was accompanied by increased contents of nutrients (ammonia and nitrate nitrogen, total phosphorus) and total iron (Table 1).

Eggs and oocytes

Egg size parameters indicated suspended solids to affect water absorption by the eggs (Table 2). Eggs incubated in filtered water showed the highest diameter, and hence the highest volume Those parameters were significantly higher than those of the eggs incubated in tap and untreated riverine water. On the other hand, no statistical differences were detected between the last two treatments (Table 2). No significant differences in oocyte size could be found between the three treatments (Table 2). As shown by the measurements, the perivitelline space formed on termination of the water absorption stage was the largest in the eggs incubated in riverine water devoid of suspended particulates (Table 2).

Table 2. Size characteristics of eggs and egg cells incubated in untreated riverine water (Treatment I) filtered water (Treatment II) and tap water (Treatment III) (mean ± standard deviation)

Treatment	Egg diameter (mm) (ANOVA p<0.01)	Egg cell diameter (mm) (ANOVA p<0.01)	Egg volume (mm3) (ANOVA p<0.01)	Egg cell volume (mm3) (ANOVA p<0.01)	Perivitelline space % (ANOVA p<0.01)
I	2.77 ± 0.059a min 2.67; max 2.90	2.44 ± 0.091a min 2.17; max 2.56	11.39 ± 0.76a min 10.04; max 12,72	7.67 ± 0.66a min 6.37; max 8,28	29,77 ± 4.19a min 20.16; max 38.28
II	2.83 ± 0.073b min 2.68; max 2.93	2. 46 ± 0.079a min 2.30; max 2.59	11.93 ± 0.90b min 10.93; max 13.19	8.10 ± 0.77a min 6.38; max 9.13	33.07± 3.22b min 26.02; max 36.79
III	2.78 ± 0.064a min 2.59; max 2.81	2.47 ± 0.080a min 2.28; max 2.51	11.24 ± 0.76a min 9.04; max 12.39	7.90 ± 0.75a min 6.21; max 9.00	29.68 ± 4.32a min 20.16; max 38.29

* means denoted with identical superscripts are not significantly different p=0.05 (Duncan's multiple range test)

Embryonic development

As shown by the observations, both the blastopore closure and eyeing occurred at the same time (at 30 and 75 D°, respectively) in all the treatments (Table 3).

The suspended solids were found to reduce duration of the embryonic development (hatching began at 95 D° and terminated at 140 D°), compared to the duration of embryogenesis in the treatments involving tap water and filtered riverine water. In addition, the hatching rate, and hence embryonic survival was reduced, too (Table 3). The fertilisation rate was at its lowest (75%) in the treatment involving water with suspended solids (Table 3).

Table 3. Duration of selected stages of embryogenesis (degree days, D°): hatching, percentage of fertilised eggs, and embryo survival rate in Treatment I (unfiltered riverine water), Treatment II (filtered riverine water), and Treatment III (tap water)

Etapy  Stages	Treatment I	Treatment II	Treatment III
Stages of embryonic development (D°)
Blastopore closure	30	30	30
Eye pigmentation	75	75	75
Duration of hatching (D°)
Commencement of hatching	95	110	100
Hatching mid-point (50% of eggs hatched)	125	130	130
Termination of hatching	140	150	158
Number of days	9.5-14	10-15	11-15
No. of eggs incubated [n]	255	310	284
% fertilisation	75	91	85
% survival	45	50	65

Larval size parameters

The final effect of exposing the eggs to suspended solids was the difference in size of the larvae hatched from eggs incubated in various treatments (Table 4).

The shortest individuals, which carried the largest yolk sacs, were those hatched from the eggs incubated in riverine water with suspended particulates (Treatment I) and in tap water (Treatment III), no significant differences in the larval length and yolk sac volume being found between treatments I and III (Table 4). Those eggs incubated in filtered water (Treatment II) gave rise to the longest larvae which carried the smallest yolk sacs. In addition, the treatment resulted in the lowest larval malformation rate (7.0%; Table 4).

Table 4. Size characteristics of pike larvae hatched from eggs incubated in riverine water (Treatment I) filtered water (Treatment II), and tap water (Treatment III) (mean ± standard deviation)

Treatment	Total length (mm) (ANOVA p<0.01)	Yolk sac volume (mm3) (ANOVA p<0.01)	% malformed larvae
I	9.34 ± 0.47a min 7.92; max 9.87	4.07 ± 0.41 b min 3.31; max 4.84	9.0
II	9.82 ± 0.29b min 9.15; max 10.29	3.77 ± 0.40 a min 2.73; max 4.61	7.0
III	9.47 ± 0.25a min 8.99; max 9.84	4.05 ± 0.42 b min 3.24; max 4.74	10.0

* means denoted with identical superscripts are not significantly different at p = 0.05 (Duncan's multiple range test)

Egg surface appearance

SEM images of the external surface of the eggs kept in untreated riverine water showed the presence of pennate diatoms, fragments of their frustules, and some other structures, both organic and inorganic in origin (Fig. 1a). No such entities were present on the surface of eggs kept in the filtered and tap water treatments. The high-magnification (x 10.000) images of those eggs incubated in filtered riverine water showed the presence of some impurities only (Fig. 1b), the surfaces of eggs kept in tap water being clean (Fig. 1c).

Fig. 1. External surface of pike eggs (x 10.000): a) incubated in untreated riverine water; b) incubated in filtered water; c) incubated in tap water

a)

b)

c)

DISCUSSION

Data on the selected water quality parameters showed the unfiltered water used in Treatment I to be characterised by increased concentrations of nutrients and total iron (Table 1). The total phosphorus concentration in the riverine water was 0.471 mgP dm^-3; although this value was only slightly in excess of the clean water standard as defined by the relevant Ministry of Environment directives [26,27], they could have affected the pike embryonic development. The iron concentration of 0.251 mg·dm^-3 was within the range reported as appropriate in the literature, safe concentrations being those below 0.35 mg·dm^-3 30]. As iron can occur in water in dissolved, colloid, or particulate form, it is evident that the water used in Treatment I contained large amounts of particulate iron. All the particulates were removed from the water by filtration, whereby the iron concentration was reduced more than eight times, which was very advantageous (Table 1). The concentration of total suspended solids in the Wiśniówka water was 20 mg·dm^-3 and met the requirements imposed by the Polish regulations mentioned above as well as the standards set by the reports of EIFAC [11] and NAS [21]. The annual mean suspended particulates concentrations in the Wiśniówka (the river having been surveyed for a few years by the Division of Environmental Sciences) were very high (65 mg·dm^-3) in 2005 and 2006, thereby failing to meet the standards as set in the Ministry of Environment Directive of 4 October 2002 [7,32]. However, from April 2007 to March 2008, the concentration of suspended solids was as low as 21 mg·dm^-3 [8]. Results of the analyses carried out in this study showed the Wiśniówka water to have improved in terms of its concentration of suspended particulates.

Analysis of suspended solids' effects on juvenile and adult salmonids, presented by Newcomb and Jensen [22] showed the concentrations of 20–25 mg·dm^-3 to have no adverse effects. A different picture emerged when eggs and larvae were exposed to suspended solids at those concentrations; even lower concentrations (10–20 mg·dm^-3) could have increased embryo mortality or at least reduce the size of embryos. As shown by this study, total suspended solids at a concentration of 20 mg·dm^-3 do affect the pike embryogenesis, the effects being visible as early as during egg fertilisation, water absorption, and embryo development. Suspended solids, even at a low concentration (close to 25 mg·dm^-3), may interfere – by settling on the egg surface – with egg fertilisation and water absorption, the net result being evident as a lowest fertilisation rate recorded in the eggs subjected to the riverine water treatment (Table 2) as well as the lowest egg volume, and hence the smallest perivitelline space, observed in that treatment, too (Table 1). In their turbidity test performed on rainbow trout eggs, Wojtczak et al. [37] observed effects of water turbidity caused by yolk lipoprotein precipitation and found the suspended particulates to be a physical factor interfering with fertilisation, most probably by affecting sperm motility and contributing to changes in micropyle canal lumen.

The shorter duration of embryonic development in the pike eggs exposed to the riverine water treatment may be also explained by invoking the embryo's need to leave the egg as soon as possible, as the oxygen availability in the water containing various suspended particulates (including unicellular algae, inorganic and organic particles, including bacteria attached to the egg surface) was reduced. Bacteria from the suspended solids, present on the egg surface, may damage the egg membrane, which may harm the egg and thereby lead to moribund or malformed embryos. Barker et al. [1] demonstrated a relationship between the density of bacteria on the egg surface and the embryo survival rate. Some eggs showed as many as 500 bacterial colony forming units (CFU) on 1 mm² egg membrane surface [1].

The tap water (control treatment) used in the laboratory to incubate eggs of various fish species [12,18] showed somewhat different levels of water quality parameters, compared to the riverine water (Table 1). Perhaps the suitably low nutrient and iron concentrations as well as the twice as high chloride content inhibited bacterial growth, whereby the egg fertilisation and embryo survival rates (85 and 65%, respectively) were high and fairly high, respectively, comparable to the results of the filtered water treatment (Table 2). Barker et al. [2] recommend that, during artificial fertilisation, the eggs – when absorbing water (egg membrane hardening) – be kept in very clean water; in our study, the filtered riverine water and tap water proved very clean.

As seen from the above, suspended solids present in water and capable of settling on fish egg surface adversely affect oxygen regime and contribute to increased nutrient concentrations. This, in turn, affects the processes involved in embryogenesis, which leads to reduced larval size and increased proportion of malformed larvae (Table 4).

To sum up, it may be contended that total suspended solids present in water are, in addition to other important environmental factors such as temperature, pH, dissolved oxygen content, and nutrient concentrations, may – even when present at low concentrations (safe for adult fish) – disturb the embryonic development of fish under natural conditions and in fish cultures. Therefore, concentrations of suspended particulates in water used for fish grow-out and farming should be kept at a suitable level by using filtering devices such as filters, sieves, microsieves [31], and the most recent membrane technologies [9,13,33,34].

CONCLUSIONS

1. The riverine water concentration of suspended solids of 20 mg·dm^-3 affects the embryonic development of pike by decreasing the fertilisation success and embryo survival rates and by reducing the duration of embryogenesis.

2. Particles settling on the egg surface adversely affect the oxygen regime inside the egg, causing the newly hatched larvae to be smaller, to carry larger yolk sacs, and to suffer of an increased rate of body malformations.

3. Increasing concentrations of total suspended solids in water are accompanied by elevated contents of nutrients and total iron.

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Accepted for print: 17.02.2011

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Małgorzata Bonisławska
Department of Aquatic Sozology, West Pomeranian University of Technology in Szczecin, Szczecin, Poland
Kazimierza Królewicza 4B
71-550 Szczecin
Poland
email: Malgorzata.Bonislawska@zut.edu.pl

Krzysztof Formicki
Division of Hydrobiology, Ichthyology and Biotechnology of Biotechnology of Reproduction,

West Pomeranian University of Technology in Szczecin, Szczecin, Poland
K. Królewicza 4
71-550 Szczecin
Poland
email: Krzysztof.Formicki@zut.edu.pl

Izabela Smaruj
Division of Hydrobiology, Ichthyology and Biotechnology of Biotechnology of Reproduction,
West Pomeranian University of Technology in Szczecin, Szczecin, Poland
K. Królewicza 4
71-550 Szczecin
Poland

Joanna Szulc
Division of Hydrobiology, Ichthyology and Biotechnology of Biotechnology of Reproduction,
West Pomeranian University of Technology in Szczecin, Szczecin, Poland
K. Królewicza 4
71-550 Szczecin
Poland

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