Trace Metal Accumulation in Eggs of Wild Nile Crocodiles (Crocodylus niloticus) from Lake St Lucia, South Africa: Implications for Biomonitoring in a Global Biodiversity Hotspot.

Nile crocodiles (Crocodylus niloticus) at Lake St Lucia, South Africa, have some of the highest blood lead (Pb) concentrations ever recorded in wildlife globally. Although exposure to Pb is known to pose major risks to wildlife reproductive success, potential impacts on crocodile reproduction at Lake St Lucia have yet to be examined. In this study, we investigated the accumulation of Pb and other trace metals (Al, V, Cr, Co, Cu, Ni, Zn and Cd) in eggs (n = 20) collected from five wild crocodile nests at Lake St Lucia. All metals analysed in this study were detected in egg contents, although concentrations varied considerably among nests and within clutches. Lead was detected in the contents of all eggs, but only at relatively low concentrations (43 ± 26 ng g-1 dry weight). Although sampling limitations commonly associated with wild population surveys prevent a complete assessment of exposure variability, our findings suggest maternal transfer may not be a significant depuration pathway for Pb and females possibly clear Pb through other mechanisms (e.g. sequestration into claws, bone and osteoderms). Metal concentrations in eggshells and shell membranes were poorly correlated with concentrations measured in egg content and thus do not provide viable non-lethal indicators for monitoring metal exposure in Nile crocodiles. Intra-clutch variability accounted for a considerable proportion of the total variance in egg content metal concentrations, suggesting the "one egg" sampling strategy often applied in reptile studies may not be an effective biomonitoring tool for wild crocodilian populations. Although maternally derived Pb does not appear to present widespread toxicological concern at Lake St Lucia, adverse effects of Pb exposure on other reproductive functions (e.g. spermatogenesis) cannot be discounted and warrant further investigation.

High lead exposure and clinical signs of toxicosis in wild Nile crocodiles (Crocodylus niloticus) from a World Heritage site: Lake St Lucia estuarine system, South Africa.

Lead (Pb) exposure is a widespread wildlife conservation threat, but impacts on reptile populations remain poorly documented. In this study, we examined Pb exposure and accumulation in a wild population of Nile crocodiles (Crocodylus niloticus) at Lake St Lucia, South Africa. Recreational angling has occurred in the area since the 1930s and incidental ingestion of Pb fishing weights has previously been identified as a major source of Pb poisoning in the local crocodile population. In 2019, we sampled blood and tail fat tissues from wild (n = 22) and captive (n = 3) crocodiles at Lake St Lucia to investigate potential impacts of chronic Pb exposure on crocodilian health. Lead was detected in blood samples of all wild crocodiles, although concentrations varied widely between individuals (86-13,100 ng ml-1). The incidence of Pb poisoning was higher in male crocodiles, with mean blood lead (BPb) concentrations in males (3780 ± 4690 ng ml-1) significantly (p < 0.001) higher compared to females (266 ± 230 ng ml-1). Blood Pb concentrations were correlated with concentrations measured in tail fat tissue (n.d - 4175 ng g-1 wet wt.). Although most of the crocodiles sampled appeared to be in good physical condition, highly elevated BPb concentrations (>6000 ng ml-1) were associated with markedly suppressed packed cell volumes (4.6-10.8%) and severe deterioration in tooth condition. These findings suggest that anaemia and tooth loss may be clinical signs of long-term environmental exposure to Pb. Although previously undocumented in crocodilians, these symptoms are consistent with Pb poisoning observed in birds and mammals, and suggest that crocodilians may be more susceptible to the long-term toxic effects of Pb than previously thought. In light of these findings, we suggest that the impact of accumulated Pb on crocodilian fitness, reproduction and mortality requires urgent attention.

Organochlorine pesticide bioaccumulation in wild Nile crocodile (Crocodylus niloticus) fat tissues: Environmental influences on changing residue levels and contaminant profiles.

Biologically significant concentrations of organochlorine pesticides (OCPs) continue to be reported in wildlife populations and are of particular concern in species that occupy the highest trophic levels. Nile crocodiles (Crocodylus niloticus) are important apex predators occurring throughout much of tropical and subtropical sub-Saharan Africa, where they inhabit estuarine and freshwater habitats often impacted by contamination. In this study we examined pesticide residue accumulation in fat tissue from Nile crocodiles at Lake St Lucia, South Africa, where historically large quantities of OCPs have been used for agriculture and disease control. During 2019, we collected tail fat samples from wild (n = 21) and captive (n = 3) individuals to examine the influence of habitat, body size and sex on variations in bioaccumulation. The principal contaminant found was p,p'-DDE, a major persistent metabolite of DDT, which continues to be used in the region for combating malaria. Tissue p,p'-DDE concentrations in wild crocodiles (95-1200 ng g-1 ww) were significantly (p < 0.05) higher compared to captive individuals (23-68 ng g-1 ww) and strongly correlated (R2 > 0.70) to body length. Male (n = 14) and female (n = 7) wild crocodiles exhibited similar contaminant body burdens, however, total concentrations were substantially lower than those measured in the same population during 2016/2017. Marked differences in residue levels and profiles appear to reflect changes in food availability and dietary exposure associated with a shift in environmental conditions. These findings suggest that periods of environmental stress may be associated with enhanced toxicological risk in crocodiles. Additional work is needed to better understand contaminant accumulation and elimination mechanisms in crocodiles, and their potential effects on reproductive health.

The ecological importance of crocodylians: towards evidence-based justification for their conservation.

Large-bodied predators are well represented among the world's threatened and endangered species. A significant body of literature shows that in terrestrial and marine ecosystems large predators can play important roles in ecosystem structure and functioning. By contrast, the ecological roles and importance of large predators within freshwater ecosystems are poorly understood, constraining the design and implementation of optimal conservation strategies for freshwater ecosystems. Conservationists and environmentalists frequently promulgate ecological roles that crocodylians are assumed to fulfil, but often with limited evidence supporting those claims. Here, we review the available information on the ecological importance of crocodylians, a widely distributed group of predominantly freshwater-dwelling, large-bodied predators. We synthesise information regarding the role of crocodylians under five criteria within the context of modern ecological concepts: as indicators of ecological health, as ecosystem engineers, apex predators, keystone species, and as contributors to nutrient and energy translocation across ecosystems. Some crocodylians play a role as indicators of ecosystem health, but this is largely untested across the order Crocodylia. By contrast, the role of crocodylian activities in ecosystem engineering is largely anecdotal, and information supporting their assumed role as apex predators is currently limited to only a few species. Whether crocodylians contribute significantly to nutrient and energy translocation through cross-ecosystem movements is unknown. We conclude that most claims regarding the importance of crocodylians as apex predators, keystone species, ecosystem engineers, and as contributors to nutrient and energy translocation across ecosystems are mostly unsubstantiated speculation, drawn from anecdotal observations made during research carried out primarily for other purposes. There is a paucity of biological research targeted directly at: understanding population dynamics; trophic interactions within their ecological communities; and quantifying the short- and long-term ecological impacts of crocodylian population declines, extirpations, and recoveries. Conservation practices ideally need evidence-based planning, decision making and justification. Addressing the knowledge gaps identified here will be important for achieving effective conservation of crocodylians.

Accumulation of organochlorine pesticides in fat tissue of wild Nile crocodiles (Crocodylus niloticus) from iSimangaliso Wetland Park, South Africa.

Nile crocodiles (Crocodylus niloticus) are important apex predators in many tropical and subtropical aquatic habitats throughout much of sub-Saharan Africa. In South Africa, large crocodile populations inhabit lakes and wetlands that are impacted by organochlorine pesticides (OCPs). Despite the continued use of these compounds and their potential adverse effects on key wildlife populations in southern Africa, limited ecotoxicoloigcal data exist. In this study, we examined the accumulation of OCPs in fat tissues of live, wild Nile crocodiles from iSimangaliso Wetland Park, a region of significant biological importance. All samples (n = 15) contained multiple contaminants in highly elevated concentrations, with total residue burdens varying between 3600 and 8000 ng g-1 ww. DDT and its metabolites were the dominant compounds detected in most samples, with ∑DDT concentrations ranging between 520 and 3100 ng g-1 ww. Elevated levels of other OCPs were also detected, including lindane (67-410 ng g-1 ww), aldrin (150-620 ng g-1 ww) and heptachlor (170-860 ng g-1 ww). Our findings show that crocodiles are exposed to OCPs throughout their range within iSimangaliso Wetland Park and contain some of the highest concentrations ever recorded in crocodilian tissue. Results indicate the need for a greater understanding of the impacts of OCP exposure and toxicological responses in crocodiles from iSimangaliso, and in Nile crocodile populations in general. The novel surgical technique described in this study provides an effective method for assessing relationships between contaminant body burdens and their potential reproductive and developmental consequences in crocodilians.

Nest-site selection, nesting behaviour and spatial ecology of female Nile crocodiles (Crocodylus niloticus) in South Africa.

Nesting biology and ecology have been investigated for Nile crocodiles (Crocodylus niloticus), but information on behaviour and movement patterns of nesting females during nest guarding is scant. Consequently, we investigated the home ranges, nest-site selection strategies, movement patterns, activity levels and nest fidelity of four nesting females using telemetry. Gravid females selected winter basking/breeding areas close (351±2m) to nest-sites. Mean home range and core-use areas of nesting females were 8539±4752m2, and 4949±3302m2 respectively. Mean home range (0.85ha) was significantly smaller than those of non-nesting females (108.4ha) during nesting season. Activity levels and mean daily movements while nesting were 8.1±2.5% and 213±64m, respectively, and increased to 47.9±11.7% and 2176±708m post-nesting. Overall levels of nest fidelity were 82.8±11.7%, (day 78.1±15.9%; night 87.3±7.8%). Highest nest fidelity recorded during incubation was 99.7% over 96days. Telemetry data from nesting females were helpful for elucidating spatial and behavioural patterns during the nest guarding period, and provided novel insights into this biologically important event.

Nest predation and maternal care in the Nile crocodile (Crocodylus niloticus) at Lake St Lucia, South Africa.

Information regarding nest predation, nest abandonment, and maternal care in the Nile crocodile (Crocodylus niloticus) is largely restricted to anecdotal observations, and has not been studied quantitatively. Consequently, we investigated their nesting biology using camera-traps over four years at Lake St Lucia, South Africa. We obtained 4305 photographs (daylight captures=90.1%, nocturnal=9.9%) of 19 nest-guarding females. Of 19 monitored nests, 37% were raided by predators (mean=12.1±6.2days subsequent to camera placement). All females returned to their nests following first predation, and on average returned three times between predator raids before nest abandonment. Water monitors (Varanus niloticus) and marsh mongoose (Atilax paludinosus) were the main egg predators. Nesting raids lasted 5.9±1.6days. Diurnally females were seldom on the nest, except during cool/cloudy weather or rain, preferring to guard from nearby shade. Females defended nests aggressively against non-human intruders. Five Nile crocodile females were observed liberating their hatchlings from nests. A detailed sequence of a mother excavating and transporting hatchlings revealed 13 excursions between nest and water over 32.5h. This, after months of continual nest attendance and defence, is illustrative of the high level of maternal care in Nile crocodiles. Camera-trapping is an effective, non-invasive method for further crocodile nesting behaviour research.

Blood lead concentrations in free-ranging Nile crocodiles (Crocodylus niloticus) from South Africa.

Generally crocodilians have received little attention with regard to the effects of lead toxicity despite their trophic status as apex, generalist predators that utilize both aquatic and terrestrial habitats, thereby exposing them to a potentially wide range of environmental contaminants. During July-October 2010 we collected whole blood from 34 sub-adult and adult free-ranging Nile crocodiles (Crocodylus niloticus) from three separate populations in northeastern South Africa in order to analyze their blood lead concentrations (BPb). Concentrations ranged from below detectability (<3 µg/dL, n = 8) to 960 µg/dL for an adult male at the Lake St Lucia Estuary. Blood lead concentrations averaged 8.15 µg/dL (SD = 7.47) for females and 98.10 µg/dL (SD = 217.42) for males. Eighteen individuals (53 %) had elevated BPbs (≥10 µg/dL). We assessed 12 general linear models using Akaike's Information Criterion (AIC) and found no significant statistical effects among the parameters of sex, crocodile size and population sampled. On average, crocodiles had higher BPbs at Lake St Lucia than at Ndumo Game Reserve or Kosi Bay, which we attribute to lead sinker ingestion during normal gastrolith acquisition. No clinical effects of lead toxicosis were observed in these crocodiles, even though the highest concentration (960 µg/dL) we report represents the most elevated BPb recorded to date for a free-ranging vertebrate. Although we suggest adult Nile crocodiles are likely tolerant of elevated Pb body burdens, experimental studies on other crocodilian species suggest the BPb levels reported here may have harmful or fatal effects to egg development and hatchling health. In light of recent Nile crocodile nesting declines in South Africa we urge further BPb monitoring and ecotoxicology research on reproductive females and embryos.