Comparative bioaccumulation of trace metals in Penaeus stylirostris in estuarine and coastal environments

Estuarine, Coastal and Shelf Science (1995) 40, 35--44

Comparative Bioaccumulation of Trace Metals in Penaeus stylirostris i n E s t u a r i n e and Coastal E n v i r o n m e n t s

F. P ~ i e z - O s u n a a n d C. R u i z - F e r n ~ i n d e z Laboratorio de Quimica Marina, Instituto de Ciencias del M a r y Limnologia, Universidad Nacional Aut6noma de MJxico, Apdo. Postal 811, Mazatl&n 82000, Sinaloa, M~xico Received 8 March 1993 and in revised form 3 January 1994

Keywords: trace metals; Penaeus s~ylirostns; body size; life-cycle; Pacific coast of M~xico Trace metal concentrations (Fe, Mn, Ni, Cu, Co, Cd, Cr and Zn) have been measured in estuarine and marine shrimp P. stylirostris collected in the Pacific coast of M6xico. Estuarine individuals (juveniles) had higher concentrations of Fe and Mn than marine individuals (adults). Size-dependent relationships were observed and differed among the elements examined. A negative slope was found for Co, Fe, Mn and Ni in estuarine juvenile shrimps, while for Cu the opposite tendency occurred. In marine adults a positive slope was observed for Cd, Co, Cr and Cu. These findings may be due to two factors: (1) that P. stylirostris spends part of its life-cycle in estuarine/lagoon environments where it is more likely to be exposed to higher levels of bioavailable trace metals (natural and anthropogenic contributions) and/or (2) different metabolic requirements of young and older specimens, which is especially applicable to copper.

Introduction Penaeus stylirostris S t i m p s o n a n d P. vannamei B o o n e s u p p o r t c o m m e r c i a l s h r i m p fisheries in lagoons o f the Pacific coast o f M~xico a n d in s o m e m o n t h s are i m p o r t a n t in the coastal trawler s h r i m p fishery ( M e n z & Bowers, 1980). T h e blue s h r i m p P. s~ylirostris is a tropical species geographically d i s t r i b u t e d f r o m M 6 x i c o ' s Baja California to Paita, Peril ( D o r e & F r i m o d t , 1987; H e n d r i c k x , in press), a n d has a life-cycle typical o f p e n a e i d s h r i m p w h i c h s p e n d p a r t o f their life in b r a c k i s h w a t e r ( E d w a r d s , 1978; G a u d y & Sloane, 1981). S p a w n i n g occurs in the sea w h e r e d e v e l o p m e n t p r o c e e d s to p o s t - l a r v a e w h i c h t h e n e n t e r estuaries a n d brackish w a t e r areas (coastal lagoons a n d tidal channels). A juvenile g r o w t h p h a s e follows, after w h i c h e m i g r a t i o n to the sea occurs. M e t a l a c c u m u l a t i o n b y m a r i n e invertebrates is influenced b y a n u m b e r o f intrinsic (e.g. size, age a n d sex) a n d extrinsic factors (e.g. m e t a l s p e c i a t i o n a n d salinity; Powell & W h i t e , 1990). T h i s w o r k a t t e m p t s to investigate the general thesis that b o d y size is one factor that affects c o n c e n t r a t i o n s o f trace m e t a l s in organisms. T h i s p a p e r presents d a t a on the levels o f F e , M n , N i , Cu, Co, C d , C r a n d Z n in P. stylirostris p o p u l a t i o n s f r o m two 0272-7714/95/010035+ 10 $08.00/0

© 1995 Academic Press Limited

36

F. P~z-Osuna & C. Ruiz-Fern~ndez

llOOW I

108° I

!

!

106 ° I

|

25°N

Mexico

lifornia

24°

23° Caimanero Lagoon

22 ° River

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a.oo.I

£1

40' Pacific Ocean 20 °

30' 10'

106°

50'

Figure 1. Collection sites (A, B) in the Pacific coast of M6xico.

sites (estuarine a n d coastal) on the M e x i c a n Pacific coast. A d d i t i o n a l l y , the relationship between trace metal c o n t e n t and b o d y size is examined.

Methods

Sampling T w o p o p u l a t i o n s of blue shrimp P. srylirostris were collected from the M e x i c a n Pacific coast in a u t u m n 1991 in two different u n p o l l u t e d areas. F i g u r e 1 shows the survey location. T h e lagoonal p o p u l a t i o n was s a m p l e d n e a r the m o u t h o f the coastal lagoon system n a m e d Teacapfin (A) (22039'N, 105°42'W) a n d the m a r i n e p o p u l a t i o n in one site (B) (21°37'N, 105°58'W) located on the n o r t h - w e s t N a y a r i t continental shelf. T h e organisms were collected b y two ways: (1) in the lagoon system with a 2 - m - r a d i u s plastic cast net, and m e s h size 10 m m (' atarraya '), a n d (2) on the c o n t i n e n t a l shelf b y t o w i n g a net trawl. T h e lagoonal-estuarine collection was c o m p o s e d o f juvenile shrimps, while the m a r i n e collection was o f adults. T h e samples o f juvenile s h r i m p s were i m m e d i a t e l y rinsed with lagoonal water a n d refrigerated ( 4 - 1 0 °C) in the field, t h e n they were t r a n s p o r t e d to the l a b o r a t o r y in p r e - c l e a n e d polyethylene containers ( M o o d y & L i n d s t r o m , 1977) to be frozen. T h e a d u l t groups were frozen in the field ( - 30 °C), i m m e d i a t e l y after they were rinsed with seawater. B o t h s h r i m p s a m p l e s were m a i n t a i n e d

Trace metals in shrimp

37

at - 20 °C for 1 or 2 weeks until analysis. Taxonomic identification and sex separation of individuals was made by examination of morphologic characteristics (Young & Reinoso-Naranjo, 1983). While choosing shrimp for the preparation of composite samples, emphasis was placed on organisms of nearly equal length. Shrimps were grouped by size into batches: 6-7 cm (6"5 ± 0 - 2 ) , 7-8 cm (7.6 ± 0.3), 8-9 cm ( 8 - 4 + 0 - 4 ) , 10-11 cm (10-7 ± 0 - 3 ) and 17-18 cm (17.7 ± 0.4) for estuarine specimens; 19-20 cm (19.5 ± 0.3) males, 19-20 cm ( 1 9 - 4 ± 0 . 5 ) females, 20-21 cm ( 2 0 . 6 + 0 . 4 ) males, 20-21 cm ( 2 0 - 7 ± 0 . 4 ) females, 21-22 cm (21-5 ± 0.5) and 23-24 cm (23-5 ± 0.6) for the marine specimens. T h e length of the specimens was determined by measuring individuals from the rostrum to the extreme of the telson. Separation of males from females was made only with the adult individuals of the 19-20 and 20-21 cm range groups. Each group contained 20-25 individuals. T h e y were dissected, using acid-washed (Moody & Lindstrom, 1977) plastic instruments, keeping only the muscle.

Chemical analysis Each composite sample of muscle tissue was dried to constant weight at 60 °C. Pulverization and homogenization were achieved by grinding in a Teflon mortar. Samples were digested with concentrated quartz-distilled nitric acid using the multiple standard addition method and the metal concentrations were determined by flame atomic adsorption spectrophotometry (Pfiez-Osuna et al., 1993). Procedural blanks were prepared and analysed with the samples. T h e performances of the method were evaluated by analysing a shrimp (Penaeus duorarum) MA-A-3FFM homogenate supplied by the International Laboratory of Marine Radioactivity (IAEA, Monaco). T h e concentrations of Cu, Cd, Cr, Ni, Fe and Zn for the standard homogenate, were in the acceptable range (twice the reported standard deviation) reported for this sample (IAEA, 1987). Manganese was underestimated; the recovery was 67%. No standard h o m ogenate data were available for Co, Ag and Pb. T h e coefficient of variation of the analysis varied with the element from 0.4% for M n to 12% for Zn. All metal concentrations were expressed as jag g - i dry weight. Trace metal concentration differences between shrimp were compared by Student's t-test (Miller & Miller, 1988). Linear, semi-logarithmic and log-log regressions were used to express size-related variations in metal concentrations.

Results a n d d i s c u s s i o n

Iron and Zn were the most abundant elements in both estuarine and marine populations, closely followed by Cu (Table 1). Manganese preceded Ni, Co and Cd. In all groups Cr was the least abundant element detected, while concentrations of Ag and Pb were consistently below the limits of analytical detection (0" 10 and 0.05 jag g - 1, respectively). In this section these results are compared with some reported studies. However, regional comparisons of results must be made with caution because of variations in the analytical and sampling procedures. Intercomparison exercises on trace elements in shrimp homogenate revealed rather poor agreement among participating laboratories (IAEA, 1987), particularly with regard to Co, Pb and Ni. Zinc concentrations found in the muscle tissue of P. stylirostris were higher (47.8-122.3 jag g 1) than in most other Pacific shrimps studied previously, such as

38

F. Pdez-Osuna & C. Ruiz-Ferndndez

TABLE 1. Mean (:k SD) concentrations of trace metals in two populations of P. stylirostris. The estuarine population includes juveniles (n=5), and the marine population includes adults (n=6) Concentration ~g g- 1) Metal Cu Mn Cd Co Cr Ni Fe Zn

Estuarine

Marine

21.2 ± 9"3 4-2* ± 2.3 0-44 ± 0-12 1-08 ± 0-81 0.72 ± 0.42 1-72 ± 1-24 133"* ± 32 83.7 ± 20"9

36-6 ± 17.6 1.4* ± 0.8 0"61 ± 0.40 0-42 ± 0"23 0.29 ± 0-24 0.72 ± 0.20 41"* ± 22 74-6 ± 25-9

Significantly different at *95% and **99% levels.

Penaeus monodon, Penaeus merguiensis (Darmono & Denton, 1990), Pandalopsis dispar, Pandalus borealis, or Pandalus platyceros (Harding & Goyette, 1989). Copper levels are known to vary widely between crustacean species (Eisler, 1981), although the concentrations found in P. scylirostris (13"9-70"3 lag g - i) were comparable to the Australian shrimp P. merguiensis and P. monodon (Darmono & Denton, 1990), and the brown and rock shrimp from the U.S. (Texas) continental shelf (Horowitz & Presley, 1977). Cadmium and Cr, non-essential elements, were found in both populations of P. stylirostris at levels similar to those in the shrimp listed by Eisler (1981). The maximum Cd concentration (1"31 lag g - 1) was measured in the largest (23-24 cm) adults. The maximum Cr concentration (1.34 lag g - 1) in the 8-9 cm juveniles, does not exceed the maximum concentration (2-8 lag g - 1) given for shrimp (Eisler, 1981). The estuarine population of P. scylirostris had more elevated Fe concentrations (94.7-177.6 lag g - 1) than reported in the literature (i.e. Ishii et al., 1978; Eisler, 1981); only Carcinus maenas (Lande, 1977) had higher concentrations. The marine population of P. stylirostris, had Fe levels (20-8-71.6 lag g - 1 ) similar to the rock shrimp from the U.S. (Texas) continental shelf (Horowitz & Presley, 1977). Manganese concentrations in both estuarine and marine populations of shrimp P. s~ylirostris (2"35-8-58 lag g - i in juveniles; 0.73-2.73 lag g - ~ in adults) were comparable to shrimp from the Australian Pacific coast (Darmano & Denton, 1990) and shrimp from the U.S. (Texas) continental shelf (Horowitz & Presley, 1977). In general, large variations appear to be evidenced in Ni between species of Crustacea (Eisler, 1981), although for shrimp the available information is limited. Nickel concentrations in P. stylirostris (0"57-3-32 lag g - 1 in younger and 0.42-0-97 lag g - 1 in older individuals) were comparable to rock shrimp (Horowitz & Presley, 1977). Comparisons were made between average metal concentrations of P. stylirostris collected from estuarine and marine sites. The average concentrations of all detectable elements except Fe and Mn in the muscle tissue of shrimps from both sites were not significantly different. Shrimp from the estuarine site contained significantly (P<0-05) higher levels of iron and manganese than shrimp from the continental shelf (Table 1). Comparing males and females, of the 19-20 and 20-21 cm size groups, female P. scylirostris contained higher concentrations of Mn, Fe and Cr (Figure 2), indicating that these elements may possibly be related in a quantitative way to gametogenesis.

Trace metals in shrimp

39

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Figure 2. Relationships between metal concentration and body size in P. srylirostris. 0 , Estuarine (juvenile) shrimp; ©, marine (adult) shrimp. F, Female shrimp; M, male shrimp. Values are means; n=3.

40

F. Pfiez-Osuna & C. Ruiz-Fernfindez

Frenet and Alliot (1985) found that females of the decapod crustacean Palaemonetes vaHans accumulate more Fe than males, while no differences were noted in Zn and M n concentrations. These results are partially in concordance with those obtained for P. stylirostris. An analysis of correlation coefficients between metal pairs in P. svylirostris revealed population-location-dependent differences. A highly significant (P<0.01) correlation was noted for the following assemblages of metals: C u - C d in the marine population and C u - C d , Co-Fe, Cr-Ni and M n - F e in both estuarine and marine populations. A significant (P<0-05) correlation was found for the following pairs of metals: C d - C o , Cu-Cr, C u - Z n in the marine population; F e - C o in the esruarine population; and Cr-Zn, C u - M n and C o - M n in both populations. Mason and Simkiss (1983) have suggested that a consistent association between particular groups of metals can be regarded as indicative of particular biochemical pathways. The relationships between metal concentrations and body size are presented in Figure 2 and results of regression analysis are given in Table 2. It can be seen that body size accounts partly for the variability observed for some elements. Different types of correlations were found for seven of the eight elements evaluated. The Fe, Mn, Ni and Co concentrations of estuarine and marine populations were correlated negatively with body size, but for Co the slope changed from negative to positive for the marine population (adult individuals) when it was considered separately (Figure 2). In contrast, Cu concentrations in both populations were associated positively with size, with a notable difference in slopes for the two populations. In the juvenile group, Cd and Cr had no significant correlation with size, but in the marine adult group a linear positive correlation was observed (Figure 2). Although a limited number of shrimp samples was evaluated (juveniles, n= 5; adults, n= 6), size-dependent relationships were apparent in P. stylirostris populations for some of the elements examined. While the direct causes for the observed slopes must remain speculative, some functional or environmental significance may be presented to account for the observed relationships. According to the metal and population examined, two different types of relationships were obtained. (1) Straight lines where the function M = m L + b described the best relation between the levels of metals in the shrimp (M) and the body length (L) and m and b are constants. Examples are: Fe and Mn over the whole size range (including juveniles and adults); Cd and Cr over the marine adult population; and Cu in the juvenile esmarine population (Table 2). (2) Curves where the power function (double log regression) M =aL/~ and or semi-logarithm M =rLn L +e is the best description of the relation. Examples are: Co, Cu and Ni for all shrimp sizes; Co and Cu in estuarine juvenile shrimp; and Cu in marine adult shrimp. It should be pointed out, that the R 2 values fitted for Co in the marine shrimp population (B in Table 2) were the same for the three curves considered. The existence of different families of curves according to the metal and population examined, possibly indicates differences in metabolism for each element and population referred. However, the differences in the behaviour of different metals reveals a more complex situation. Table 2 provides more details of the best fit regressions for linear, power and semi-logarithm models. The slopes of the regressions of metal content (particularly Co and Cu) against size varied depending on the range in body size, which is probably determined by both life-cycle and environmental factors. The shrimp P. srylirostris spends the early part of its life-cycle in estuarine-lagoon environments where it is more likely to be exposed to higher levels of both natural and man-introduced trace metals. The change of slope or

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( M ) a n d b o d y s i z e ( L ) in P. stylirostris. ( A ) E s t u a r i n e s h r i m p p o p u l a t i o n l a r g e r t h a n 19 c m ( n = 6 ) . ( C ) ( A ) + ( B ) ( n = 11)

- 4"72

shrimp population

R is t h e c o r r e l a t i o n c o e f f i c i e n t ; m , b, a , r , 6, a n d e a r e t h e c o e f f i c i e n t s o f t h e e q u a t i o n s Correlations are significant at *95%, **98% and ***99% levels. --, Not significant.

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Size

long (n=5).

TABLE 2. R e g r e s s i o n a n a l y s i s o f t r a c e m e t a l c o n c e n t r a t i o n

4.82

7-06

354.98

- 24.66 - 684.18 - 30.00

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42

F. Pdez-Osuna & C. Ruiz-Ferndndez

disruption of the tendency in the relationships between Cd, Co, Cr and Cu occurs when the shrimp becomes capable of reproduction as an adult (length >19 cm); the gonad development and biochemical variations associated with reproduction, rather than with the body size, appears to be an important source of variation in the bioaccumulation of these trace metals. The absence of an observed significant correlation in Zn (Figure 2, Table 2) may be because P. stylirostris shows a certain ability to regulate internal Zn concentrations, and that the body size and biochemical factors have small or null influence on the Zn variability. Besides, the high baseline tissue concentration of Zn could conceal low changes in shrimps exposed to increasing environmental levels. In crabs and shrimps studied under experimental conditions of low salinity, maximum accumulated concentrations of Cd have been observed (Eisler, 1981). Between estuarine and marine populations of P. s(ylirostris no significant differences in Cd (Table 1) were noted; this apparently reveals that temporal low salinity, which is exposed to the juvenile shrimp, appears to have little or no influence in the bioaccumulation of Cd, in contrast with experimental results mentioned previously. The significance of salinity as a factor in the bioaccumulation of trace metals appears to be more viable to explain the relationships of the negative slope for Co, Cr, Fe, Mn and Ni (Figure 2), which could be due to bioavailability difference in a variable salinity environment than to actual exposure to higher metal concentrations. The concentrations of trace metals in the tissues of marine invertebrates depend on the accumulation strategy adopted by each species for each metal. The accumulation strategy results from the net difference between rates of uptake and excretion of metal, as affected by changes in body tissue. Relative rates of metal uptake and excretion are affected by features of the biology of the organism, including the permeability of external surfaces, the nature of the food, and efficiency of osmoregulatory systems present (Rainbow, 1990). The diet of many species of shrimps changes significantly with size or age. There appear to be two main reasons for this (Dall et al., 1990), first a change in habitat as they grow, and second a switch away from a juvenile diet incorporating plants to an adult diet that may be predominantly carnivorous. This applies to P. stylirostris; unfortunately, specific information about the juvenile and adult diets in this species is non-existent. The existence of age- and size-dependent metal accumulation by aquatic biota has been documented by several investigators, particularly for marine and estuarine molluscs (Boyden, 1977; Cossa er al., 1980; Lacerda et al., 1983; Strong & Luoma, 1983; Amiard et al., 1986). In crustaceans the information available in this context is more limited. Martin (1974) analysed nine elements in whole-body samples of the crab Cancer irrorarus. Only Mn exhibited a significant correlation with body size, concentrations increasing with size. Rainbow and Moore (1986) found that the concentrations of Cu, Fe, Pb and Zn in amphipods were significantly affected by body size, with smaller individuals having the highest concentrations. Krantzberg (1989) studied the effects of age and body weight on metal accumulation in the larvae of the insect Chironomus, and observed that the slopes of the regressions of metal burdens against age and size varied depending on the range in body size considered. Among fourth instar larvae, younger chironomids had higher concentrations of Cd, Mn, Ni, Fe and Cu than older instars. These results are partially concordant with those obtained for P. s~ylirostris. Darmono and Denton (1990) recently found that the levels of M n in muscle tissue of the shrimp species P. monodon and P. merguiensis tended to be higher in smaller

Trace metals in shrimp

43

individuals. Similarly, Garcia a n d F o w l e r (1972) f o u n d that levels of Co, Cr, C u , M n a n d Z n in the shrimp Penaeus californiensis showed the same tendency. T h e s e observations coincide with the b e h a v i o u r of M n , C r and C o in P. stylirosrris, b u t c6ntrast with Cu.

Conclusions I n general, the trace metal variations reported here t e n d to fall within the ranges of similar organisms collected elsewhere. It is interesting to note, however, that there are significant differences b e t w e e n metal c o n c e n t r a t i o n s in m a r i n e a n d estuarine-lagoon shrimps. T h e metal levels of F e a n d M n in the estuarine juvenile shrimps were higher t h a n in the m a r i n e adult shrimps. S i z e - d e p e n d e n t relationships exist to P. stylirostris a n d differ a m o n g the elements examined. Cobalt, Fe, M n a n d N i were correlated negatively with b o d y size, b u t with C u the opposite t e n d e n c y was observed. T h e different patterns m a y reflect different metabolic d e m a n d s for distinct elements; alternatively, juvenile shrimp (small size) could be exposed to higher c o n c e n t r a t i o n s of bioavailable trace elements in estuarine e n v i r o n m e n t s , particularly as they progress from adolescents to juveniles. Body size a n d biochemical changes associated with growth could be a source of significant variation in trace metal c o n c e n t r a t i o n s (especially for Co, Cu. a n d Fe) in P. stylirostris.

Acknowledgements T h i s work was c o n d u c t e d with fi.mding by research grant from the C o n s e j o N a c i o n a l de Ciencia y T e c n o l o g i a ( C O N A C Y T ) t h r o u g h the project 0 6 2 5 - N 9 1 1 0 . T h e authors t h a n k H. M. Zazueta-Padilla, H. Boj6rquez-Leyva, S. G u e r r e r o - G a l v f i n a n d A. N u f i e z - P a s t r n for their assistance in the laboratory a n d to the referee C a i n for his help a n d critical review of the m a n u s c r i p t .

References Amiard, J. C., Amiard-Triquet, C., Berthet, B. & Metayer, C. 1986 Contribution to the ecotoxicological study of cadmium, lead, copper and zinc in the mussel Mytilus edulis. I. Field study. Marine Biology 90, 425-431. Boyden, C. R. 1977 Effect of size upon metal content of shellfish.Journal of the Marine Biological Association of the United Kingdom 57, 675-714. Cossa, D., Bourget, E., Pouliot, D., Piuze J. & Chanut, J. P. 1980 Geographical and seasonal variations in the relationship between trace metal content and body weight in Mytilus edulis. Marine Biology 58, 7-14. Dall, W., Hill, B. J., Rothlisberg, P. C. & Sharpies, D. J. 1990 The Biology of the Penaeidae. Academic Press, San Diego, 489 pp. Darmono, D. & Denton, G. R. W. 1990 Heavy metal concentrations in the banana prawn, Penaeus merguiensis, and leader prawn, P. monodon, in the Townsville region of Australia. Bulletin of Environmental Contamination and Toxicology 44, 479-486. Dore, I. & Frimodt, C. 1987 An Illustrated Guide to Shrimp of the World. Osprey Books, Huntington, New York and Scandinavian Fishing Year Book, Hedehusene, Denmark, 229 pp. Edwards, R. R. C. 1978 The fishery and fisheries biology of penaeid shrimp on the Pacific coast of Mexico. Oceanography and Marine Biology Annual Reviews 16, 145-180. Eisler, R. 1981 Trace Metal Concentrations in Marine Organisms. Pergamon Press, New York, 687 pp. Frenet, M. & Alliot, A. 1985 Comparative bioaccumulation of metals in Palaemonetes varians in polluted and non-polluted Environments. Marine Environmental Research 17, 19-44. Garcia, A. P. & Fowler, S. W. 1972 Anfilisis de microelementos en invertebrados marinos del Golfo de Califomia. Memorias del IV Congreso Nacional de Oceanografia (M~xico) , 115-I 26.

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17. P~ez-Osuna & C. Ruiz-Fern,~ndez

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