Trace elements and chlorinated hydrocarbons in eggs of Pelecanus crispus, a world endangered bird species nesting at Lake Mikri Prespa, North-western Greece

Eggs of the Dalmatian pelican, Pelecanus crispus, collected from 1984 to 1986 at Lake Mikri Prespa, north-western Greece, contained residues of trace elements and PCBs at low concentrations, and of DDE at rather high concentrations. DDE is negatively related to eggshell thickness. Eggshell thickness was reduced by 12-20% in comparison with the pre-1947 (before DDT use) eggshell thickness. However, this decrease did not affect the reproductive success of this species. The main fish species eaten by the Dalmatian pelican at Lake Mikri Prespa were analyzed for pollutants. All the fish contained low concentrations of residues. The contribution of the diet while the birds are on the wintering grounds is unknown. Recommendations for a monitoring programme of pollutants in eggs of the Dalmatian pelican, a world-endangered species, are proposed.     

Organchlorine content and shell thickness in brown booby (Sula leucogaster) eggs in the Gulf of California and the southern Pacific coast of Mexico

We determined egg concentrations of organochlorines and thickness of eggshells from brown boobies at eight colonies ranging from the northern Gulf of California to southern Mexico. The only common residue was that of DDE, which was found in almost all eggs. DDE content apparently reflected pre-1990 DDT use in nearby agricultural areas and, at one site, intensive mosquito control for high-end tourism development. There were no inter-colony differences in eggshell thickness, and variation in this variable likely reflected individual bird characteristics and/or individual feeding source. This variable was not a good proxy to DDE exposure of brown boobies, under current DDE levels in the brown booby trophic chain. In the northern Gulf of California, eggshell thickness has recovered to pre-DDT conditions. Our data indicate that the Gulf of California and southwestern coast of Mexico have a healthy near-shore marine environment, as far as organochlorines are concerned.     

Do PCBs cause eggshell thinning?

The evidence that PCBs are involved in eggshell thinning is examined. In experiments in which both PCBs and DDE were used, it was found that DDE, but not PCBs, caused eggshell thinning of mallard and American kestrel. For two other species, bobwhite and Japanese quail, no thinning was observed with either agent. Numerous other studies with DDE alone have demonstrated that this agent can cause eggshell thinning in many, but not all, species. It is concluded that DDE is the only compound that has caused significant eggshell thinning at environmentally realistic doses.     

Accumulation of organochlorine contaminants in double-crested cormorants

Cormorant eggs and lipid samples from juvenile Cormorants were analyzed for 14 organochlorine contaminants. Low concentrations (geometric mean < 0.05 microg/g) of hexachlorobenzene (HCB), lindane, oxy-chlordane, heptachlor epoxide, dieldrin, endrin, mirex, DDD and DDT in eggs primarily reflected the wintering-ground origin of organochlorine contaminants. Overall geometric mean concentrations of DDE and PCBs in Cormorant eggs were 3.90 and 2.22 microg/g egg respectively, and would not affect reproduction or eggshell thickness. Eggshells averaged 0.44 mm in thickness and no correlation (r2 = 0.17) with log-transformed DDE residues in Cormorant eggs was evident. Only DDE and PCBs were detected in lipid samples from 5- to 8-week-old Cormorants (geometric mean approximately 1.0 microg/g lipid for each compound). The PCB: DDE ratios in Cormorant lipid from some individual colonies were 2-3.5 times greater than the ratio in eggs from the same colony, suggesting an accumulation of PCBs related to local diet. Juvenile Cormorants might serve as regional indicators of chemical residue contamination in Alberta, and provide a temporal perspective on changes in contaminant burdens in aquatic ecosystems.     

Long-term trends and sources of organochlorine contamination in Canadian tundra Peregrine Falcons, Falco peregrinus tundrius

Levels of eggshell thinning, and organochlorine residues in egg contents, blood plasma of adults and juveniles, tissue samples, and prey species were determined for a population of migratory Peregrine Falcons (Falco peregrinus tundrius) breeding in the Canadian Arctic. Temporal trends were assessed by comparing data collected during 1991-1994, with data from 1982-1986, for the same population. Shells (n=54) from 1991-1994 averaged 15% thinner than eggs produced prior to the introduction of DDT. No improvement in shell thickness was detected between decades. Mean DDE residue levels in eggs showed a decline from 7.6 mg kg (1982-1986) to 4.5 mg kg (1991-1994), but there was no significant change in SigmaPCB residues. Moreover, the proportion of clutches with eggs exceeding critical SigmaPCB, DDE, and dieldrin residue levels (10%) did not change between decades. Relative to Greenland and Alaskan populations, F. p. tundrius at Rankin Inlet show high levels of organochlorine contamination and little reduction in residues over the last decade. These Tundra Peregrines continue to be exposed to organochlorines in Latin America; however, results also link relatively high levels in the study population with waterfowl species that do not leave Canada in winter.     

Trends of organochlorine residues in eggs of birds from Italy, 1977 to 1985

All the eggs, collected in Italy in 1982 and 1983, of two species of passerine birds, three gulls, four terns and the night heron, contained DDE and, with lower frequencies, other organochlorine contaminants. Organochlorines were more concentrated in the species of higher trophic level. DDE contamination showed a decreasing trend from 1978 to 1985 in one passerine, two terns and in the heron. After 1980-1982, the level of contamination was below the critical threshold beyond which reproduction is affected, eggshell thickness was only slightly or not reduced; therefore, the current impact of organochlorines on these birds is probably negligible. Detrimental effects may have occurred during the 1970s, when some of the eggs were contaminated beyond the critical threshold.     

PBDEs, PCBs, and DDE in eggs and their impacts on aplomado falcons (Falco femoralis) from Chihuahua and Veracruz, Mexico

Eggs from aplomado falcons (Falco femoralis septentrionalis) nesting in Chihuahua and Veracruz, Mexico, were analyzed for organochlorine pesticides, PCBs, and PBDEs. p,p′-DDE was the only organochlorine found in all eggs at concentrations ranging from 0.13 to 7.85 μg/g wet weight. PCBs ranged from 0.04 to 2.80 μg/g wet weight and PBDEs from 62 to 798 ng/g lipid weight. DDE concentrations in eggs were not significantly different among regions; however, PCBs were significantly greater (P = 0.015) in Tinaja Verde, Chihuahua than in the other three regions. Also, PBDEs were significantly higher (P < 0.0001) in eggs from Veracruz than in those from Chihuahua. DDE concentrations in eggs were much lower than those associated with eggshell thinning. PBDEs and PCBs were lower than those reported in raptors from industrialized countries. Overall, contaminant concentrations observed suggest no likely impact on hatching success. The PBDE concentrations are among the first to be reported in raptor species in Mexico.     

Reduced breeding success of Cormorants (Phalacrocorax carbo sinensis) in relation to persistent organochlorine pollution of aquatic habitats in The Netherlands

Cormorants (Phalacrocorax carbo sinensis) breeding in the heavily contaminated sedimentation area of the rivers Rhine and Meuse have a severely reduced breeding success as compared to several other Dutch colonies. A detailed analysis of reproductive performance in combination with chemical analysis of eggs and food from colonies in differently contaminated aquatic habitats is presented. The differences in breeding success between colonies are caused mainly in the egg-stage of breeding. Eggshell thinning and increased embryonic mortality cause the differences in hatching success. The observed effects seem to be related to chlorinated hydrocarbons. Significant correlations are found for concentrations of DDE with eggshell thinning and for concentrations of PCBs with hatching and breeding success. The correlations between concentrations of chlorinated hydrocarbons in eggs and biological effects measured in the field are established both on colony and individual clutch level.     

Effect of dietary supplementation of essential oils mixture on performance,eggshell quality,hatchability, and mineral excretion in quail breeders

The main aim of this study was to investigate the effect of six different levels (0, 50, 100, 200, 400, and 600 mg/kg) of phytogenic feed additive containing a mixture essential oils from thyme, black cumin, fennel, anise and rosemary on performance, eggshell quality, reproductive traits, and mineral excretion in quail breeders. In this trial, a total of 60 male and 120 female quails, 91 days old, were randomly distributed in six experimental groups. During the 60-day experiment period, birds were fed with six treatment diets. Performances, eggshell qualities, hatchability, and mineral excretion data were evaluated at the end of the experiment. Results showed that the different dietary levels of essential oil mixture had no significant effect on performance parameters, damaged eggs, eggshell weight, fertility, hatchability of fertile eggs, hatchability of set eggs, and lead and boron excretion. On the other hand, 50 mg/kg supplementation of essential oil mixture (EOM) significantly improved egg-breaking strength and eggshell thickness, and ash, calcium, phosphorus, magnesium, manganese, zinc, and cadmium excretion was significantly depressed in quail breeders supplemented with the two higher doses (400 or 600 mg/kg) of EOM. These results concluded that supplementing diets with EOM improved egg-breaking strength and decreased excretion of minerals in breeder quails.     

The role of DDE,PCB, coplanar PCB and eggshell parameters for reproduction in the white-tailed sea eagle (Haliaeetus albicilla) in Sweden

The reproduction of white-tailed sea eagles was monitored in 1964-1999 in 3 differently contaminated sub-populations: Baltic Sea coast (Bp), inland central Sweden (Ip) and Lapland (Lp). 249 dead eggs from 205 clutches were obtained for analyses of DDE and PCBs and for eggshell measurements. A desiccation index (Di) value was calculated for each egg as a measure of water loss through the shell. In the highly contaminated Bp, p,p'-DDE concentrations in the eggs decreased continuously and 5-fold during the study period and PCB concentrations decreased 3-fold from the mid 1980s. The PCB pattern changed slightly over time towards more high-chlorinated congeners but the relative toxicity of the PCB mixture, expressed as 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQ), remained constant and TEQ can be assumed to have decreased in a similar way as PCB over time. Productivity (P), shell thickness (St), shell index (Si) and Di increased over time in the Bp but no change in Di or productivity occurred in the Lp, where residue concentrations were 5-8 times lower. P of the Bp was not correlated to St or Si but was negatively correlated to Di, DDE and PCB. An S-shaped dose-response relationship was indicated between P and DDE. After 1988, when the PCB/DDE ratio was considerably higher than previously, PCB but not DDE concentrations were significantly higher in eggs with dead embryos as compared to undeveloped eggs, implying lethal concentrations of PCB, and a LOEL of 320 pg g-1 TEQ is suggested for embryo mortality. In a subset of 21 eggs, representing productive and unproductive females, analyzed for a selection of coplanar PCB congeners, tris(4-chlorophenyl) methanol and bis(4-chlorophenyl) sulphone, there was no evidence for a correlation between P and any of these compounds. A reduction in residue concentrations in old females did not lead to increased P or improved Di-values, indicating a remaining effect from a previous, higher exposure to contaminants. The inability to reproduce included a high rate of undeveloped eggs, indicating effects at a prezygotic stage. P showed the strongest correlation with Di, and Di was most strongly correlated to DDE. Thus, the remaining effect of previous exposure resulted in a stronger correlation to the symptom (Di) rather than to the suggested causative agent (DDE). LOEL values for depressed P were estimated at 120 micrograms g-1 DDE and 500 micrograms g-1 PCB (lipid basis). It is concluded that the major reason for depressed P during the study period was DDE, but that effects also from PCB were largely concealed by the effects from DDE.     

Organochlorines and eggshell thinning in northern gannets (Sula bassanus) from Eastern Canada, 1968-1984

The northern gannets (Sula bassanus) nesting on Bonaventure Island, Quebec, were studied from 1968 to 1984 in order to measure environmental contaminant levels and their relationship to productivity. Fresh eggs in 1969 contained a mean DDE level of 18.5 mg kg(-1) and had shells which were 17% thinner than pre-1947 samples. Unhatched eggs in 1969 had no outer calcified layer, a mean thickness 20% less than the pre-1947 mean, and mean DDE concentration of 30.6 mg kg(-1). Significantly higher levels of eight contaminants were measured in unhatched than in fresh eggs collected in 1969. DDE and shell thinning were also intercorrelated with nine other contaminants; these data strongly implicate toxic chemicals, particularly DDE, as the main cause for the low breeding success of Bonaventure gannets from 1966 to 1974. Extensive use of DDT to control forest insects around the Gulf of St Lawrence ceased in 1969. Use of DDT, dieldrin and PCBs was restricted in North America during the early 1970s. Residues of DDT, DDD, DDE, PCBs, dieldrin, HCB and chlordane-related compounds in gannet eggs decreased significantly during this study. Heptachlor epoxide remained constant while alpha-HCH appeared to increase. Estimated half-lives ranged from 3.1 years for DDD to 35.4 years for oxychlordane. The breeding success and population of the colony have coincidentally increased.     

Organochlorine and heavy metal contamination in the eggs of the Spanish Imperial Eagle (Aquila (heliaca) adalberti) and accompanying changes in eggshell morphology and chemistry

Eggs of the Spanish Imperial Eagle (Aquila (heliaca) adalberti) contained small amounts of heavy metals and organochlorine contaminants, including DDE, aldrin, dieldrin and HCHs, PCBs. Levels of organochlorine, except DDE, have decreased from 1972 to 1984. This paper reports how the structural and chemical characteristics of modern shells differ from those of older shells, unaffected by pesticides. Also, fertile and infertile recent eggs are compared. A 12.6% decrease in eggshell thickness has occurred in conjunction with a slight decrease in degree of crystallisation, but no significant changes have been found in other structural variables. The difference in chemical composition of the shell between modern and old eggs is both qualitative (presence of chlorine, potassium, magnesium and copper in recent shells) and quantitative (increase in the percentage of phosphorus and sulphur). The only clear differences between fertile and infertile eggs were a greater increase of phosphorus content and altered crystallisation in the latter. No clear relation between the amount of the mineral constituents of the shell and morphological alterations was established. The levels of contaminants in the contents seemed to be independent of the chemical alterations of the eggshell. The breeding parameters of the overall population showed no significant changes after the introduction of pesticides. However, eggshell changes have occurred in this species, which is one of the rarest birds of prey of the world, and some breeding individuals have sufficiently thin shells to suspect reduced reproductive success.     

Organochlorine contaminants and eggshell thinning in grebes from prairie Canada

Eggs of five species of grebe were collected from Manitoba, Saskatchewan and Alberta during 1982-1987: red-necked (Podiceps grisegena), horned (P. auritus), eared (P. caspicus), western (Aechmophorus occidentalis) and pied-billed (Podilymbus podiceps). DDE and PCBs were present in all samples analyzed, whereas dieldrin, mirex and oxychlordane were occasionally present at low levels. Mercury was present at low levels in all samples for which it was analyzed. Red-necked grebes nesting in Manitoba had the highest contaminant levels and, assuming that contaminant burdens were accumulated principally on the wintering grounds, the mean PCB:DDE ratio (3.1) indicated that these birds and those from sites in central and eastern Saskatchewan probably wintered on the Atlantic coast. Overall low contaminant levels and a low mean PCB:DDE ratio (1.4) in the eggs of red-necked grebes breeding in Alberta and western Saskatchewan suggested that these birds wintered on the Pacific coast. A similar pattern was apparent in horned and eared grebes. Concentrations of DDE and PCB were both significantly correlated with Ratcliffe index (shell thickness), and were strongly correlated with each other. Ratcliffe indices were determined for historical collections of red-necked grebe eggs. Eggshell thickness of grebes nesting in Manitoba declined significantly during the years following the introduction of DDT (post-1947) and has only recovered partially since it was banned in 1972. The Alberta-breeding population did not appear to have undergone any significant decrease in shell thickness.     

Chlorinated hydrocarbons and shell thinning in eggs of (Accipiter) hawks in Ontario, 1986-1989

Eggs of sharp-shinned hawks (Accipiter striatus), Cooper's hawks (A. cooperii), and northern goshawks (A. gentilis) were collected from nests in south-central Ontario from 1986 to 1989. Detectable levels of the chlorinated hydrocarbons DDE, DDT, DDD, mirex, photomirex, cis-nonachlor, trans-nonachlor, oxychlordane, dieldrin, heptachlor expoxide, HCB and PCB were present in all the eggs analyzed. Mean contaminant levels were highest in sharp-shinned hawks, slightly lower in Cooper's hawks, and significantly lower in goshawks; for example, mean DDE values were 7.23, 4.48 and 0.90 mg kg(-1) (wet weight), respectively. Total PCB levels were generally less than 1.5 mg kg(-1), lower than those associated with reproductive effects in field and laboratory studies with other species. Mean shell thicknesses of sharp-shinned and Cooper's hawk eggs were significantly less than mean pre-DDT era thicknesses (-10 and -8%, respectively), reductions that were probably not relevant to reproductive success. Goshawk eggs exhibited no significant reduction in shell thickness. Contaminant levels among the three species probably reflect differing food habits and migratory patterns.     

Chlorinated hydrocarbons in the tissues of South Polar Skuas (Catharacta maccormicki) and Adélie Penguins (Pygoscelis adeliea) from Ross Sea, Antarctica

High rates of egg infertility and embryo death in a colony of South Polar Skuas breeding in the Antarctic were similar to those in polluted North Atlantic populations of the Great Skua. Such loss could not be linked to factors such as organochlorine pollutants, as levels of DDE and PCBs in the contents of skua eggs from the population were only a small fraction of those in polluted skua populations from the Northern Hemisphere. Average eggshell thickness for skuas nesting on Ross Island has shown no significant change since the introduction of DDT. Concentrations of DDE and PCBs in South Polar Skuas were 13 and 22 times higher, respectively, than those in the eggs of sympatric Adélie Penguins, and this probably reflects the greater exposure of skuas to pollution when they migrate north of the Antarctic Convergence in winter. Residues in liver tissue showed a similar trend, and a higher rate of mixed function oxidase induction in skua liver compared to that of penguins is consistent with the trends seen in pollutant levels. The same PCB congener predominated in both skua and penguin samples. Comparisons with historical residue data suggest that global levels of DDT residues are declining.     

Organochlorine contaminants in cormorant, darter, egret, and ibis eggs from South Africa

During the last 15 years, no research has been published on the levels of pesticides in bird eggs from South Africa, despite the high levels found previously. We analysed eggs from African darter, cattle egret, reed cormorant, African sacred ibis, as well as single eggs from some other species, and found HCB, DDTs, HCHs, chlordanes and PCBs at detectable levels. The presence of mirex in all species was unexpected, since this compound was never registered in South Africa. It also seemed as if terrestrial feeding birds had higher DDE:PCB ratios when compared with aquatic feeding birds. Except for chlordane, the African darter eggs had the highest levels of all other compounds (mean 370 and 300 ng g(-1) ww Sigma pesticides and Sigma PCBs, respectively). Multivariate analysis clearly distinguished the aquatic and terrestrially feeding birds on pollution profile. The African darter (aquatic feeding) and the cattle egret (terrestrial feeding) would be good indicator candidates. Eggshell thinning was detected in the African darter, and was associated with most of the compounds, including DDE and PCBs. We raise a concern that generally longer living birds in warmer climates, laying fewer eggs per clutch, might be at increased risk when compared with trophically similar birds exposed to equivalent levels of pollution in colder climates. Given the scarcity of water and the high biodiversity in Southern Africa, climate change will exert strong pressure, and any additional anthropogenic contamination at levels that can cause subtle behavioural, developmental and reproductive changes, can have serious effects.     

Organochlorine contaminants in eggs of Common Terns from the Canadian Great Lakes, 1981

To determine if contaminant levels in Common Terns had changed over the last decade, we collected and analyzed eggs from four nesting colonies on the three lower Great Lakes during 1981. DDE and PCBs were detected in every egg from the four colonies. Dieldrin, mirex and trans-nonachlor were detected in more than 45% of the eggs. Seven other organochlorine contaminants (DDD, DDT, hexachlorobenzene, oxychlordane, cis-chlordane, cis-nonachlor and toxaphene) were detected in less than 25% of the eggs. Eggs from the Lake Ontario colony were generally the most heavily contaminated. Comparisons of DDE and PCB data with earlier studies of Common Terns indicated that contaminant levels in eggs from the four sampled colonies, or nearby sites, have decreased by up to 80-90% from 1969-1973 to 1981. Interspecies comparisons showed that Common Tern eggs have lower organochlorine residue levels than eggs of Caspian Terns or Herring Gulls. Dietary variation and migratory status are possible explanations for the differences in residue levels among species. Eggshell thickness, log-PCBs, and log-DDE were not significantly intercorrelated. Elevated contaminant levels in the early 1970s might be at least partly responsible for the decline of the Great Lakes Common Tern population over the past decade. Stabilization of population numbers during the early 1980s suggests that organochlorine pollution levels have been reduced to a point where they are no longer an important factor in the population dynamics of this species on the Great Lakes.     

Evaluation of the possible adverse effects of legacy persistent organic pollutants (POPs) on the brown booby (Sula leucogaster) along the Brazilian coast

This study aimed to investigate the impact of contamination by persistent organic pollutants (POPs) on Brazilian wildlife. The concentrations of certain POPs, including dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCBs), in the eggs of the brown booby (Sula leucogaster) were measured. The eggs were collected from breeding colonies located on three archipelagos (Saint Peter and Saint Paul, Abrolhos and Cagarras Islands) in the Atlantic Ocean, which are located at different distances from the Brazilian coast (range 4-1010 km). In addition, possible alterations in eggshell characteristics were evaluated. The average values of POPs found in eggs from the archipelago of Saint Peter and Saint Paul (0.05 μg g⁻¹ of ΣPCBs and 0.01 μg g⁻¹ of ΣDDT) and the archipelago of Abrolhos (0.19 μg g⁻¹ of ΣPCBs and 0.03 μg g⁻¹ of ΣDDT) were low compared to the reference values reported in the literature. In contrast, the concentrations measured in eggs from Cagarras (8.4 μg g⁻¹ of ΣPCBs and 1.8 μg g⁻¹ of ΣDDT) were the highest, and this total PCB level is close to the threshold values considered to be harmful to birds. Our findings indicate that the brown booby colony closest to the Rio de Janeiro coast has recently been exposed to DDT. Despite the high pollution levels found on the Cagarras Islands, no alterations in the eggshell weight or the thickness of the analyzed eggs were detected. Hence, more detailed studies are recommended to determine the actual effects of the selected POPs on the Cagarras breeding colony.     

Organochlorine contamination in the Great Crested Grebe (Podiceps cristatus): effects on eggshell thickness and egg steroid levels

Eggs of the Great Crested Grebe (Podiceps cristatus) were collected from a breeding area on Lake Maggiore (Northern Italy) from 2001 to 2005 in the vicinity of a p,p'-DDT manufacturer, whose production was stopped in 1996. DDT homologue and PCB congener levels were determined and compared to levels in eggs collected from other breeding areas on Lake Maggiore and in a presumably less contaminated area on Lake Garda. Although Lake Garda eggs on average possessed a lower level of p,p'-DDE than Lake Maggiore eggs, they had significantly higher levels of PCBs and could not be used as a reference population for the measurement of eggshell thickness. Nevertheless, a negative linear relationship was found between p,p'-DDE concentration and eggshell thickness for eggs collected from both lakes, indicating a possible causal relationship. Testosterone and 17beta-estradiol concentrations were also determined for eggs collected from both lakes in 2004. Average concentrations of both hormones were the lowest in eggs from Lake Maggiore; however, the very high variability within broods did not result in any significant difference between the lakes.     

Assessing breeding potential of peregrine falcons based on chlorinated hydrocarbon concentrations in prey

Peregrine falcons (Falco peregrinus) now breed successfully in most areas of North America from which they were previously extirpated. The loss during the mid-part of the last century of many of the world's peregrine populations was largely a consequence of impaired reproduction caused by the effects of DDE on eggshell quality and embryo hatchability. Population recovery has been attributed to re-introduction efforts, coupled with regulatory restrictions on the use of organochlorine pesticides. Peregrines have not returned to breed in some areas, such as the Okanagan Valley of British Columbia. That region has been extensively planted in fruit orchards which were treated annually with DDT during the early 1950s to the 1970s. Ongoing contamination of avian species, including potential peregrine prey, inhabiting orchards has been documented. In response to an initiative to release peregrines around the city of Kelowna in the Okanagan Valley, we collected potential peregrine prey species and analyzed whole bodies for chlorinated hydrocarbon residues. We used a simple bioaccumulation model to predict concentrations of DDE in peregrine eggs using concentrations in prey and estimates of dietary makeup as input. Peregrines would be expected to breed successfully only if they fed on a diet primarily of doves. Feeding on as little as 10% of other species such as starlings, robins, gulls and magpies would produce DDE concentrations in peregrine eggs greater than the threshold of 15 mg/kg. We also estimated the critical concentration of DDE in total prey to be about 0.5 mg/kg, one half of the previous most conservative criterion for peregrine prey. Concentrations of dieldrin and PCBs in peregrine prey are less than suggested critical levels.