Altered histology of the thymus and spleen in contaminant‐exposed juvenile American alligators

Abstract

Morphological differences in spleen and thymus are closely related to functional immune differences. Hormonal regulation of the immune system has been demonstrated in reptilian splenic and thymic tissue. Spleens and thymus were obtained from juvenile alligators at two reference sites in Florida, USA: Orange Lake and a National Wildlife Refuge, Lake Woodruff, as well as from a contaminated lake, Lake Apopka. Lake Apopka has been extensively polluted with agricultural pesticides. Tissues were prepared for histological analysis to determine if previously detected endocrine abnormalities associated with contaminant exposure might also be reflected in morphological differences in splenic and thymic structures important for immunological response. Similar tissues were taken from captive-raised juvenile female alligators (3 years old) that were hatched from eggs collected on Lake Woodruff and Lake Apopka. Differences in thymic ratios (medulla/cortex) were found among alligators collected from the two lakes (P = 0.0051). Alligators from Lake Apopka had smaller thymic ratios than animals from either reference lake. Males from Lake Woodruff had significantly smaller lymphocyte sheaths in the spleen than females (P = 0.0009), indicative of a normal sexual dimorphism. Lymphocyte sheath width differed among females obtained from the three lakes, with females from Lake Apopka having the smallest sheath width and those from Orange Lake having the largest. Malpighian body area was largest in alligators from Orange Lake, intermediate in Lake Woodruff, and smallest in Lake Apopka. In contrast to that observed for wild-caught animals, no difference was found in the thymic medulla/cortex ratio of captive-raised female alligators (P = 0.378). Captive-raised female alligators from Lake Apopka and Lake Woodruff displayed lake-associated differences in lymphocyte sheath width as observed in wild animals; Lake Apopka alligators had smaller lymphocyte sheath width compared to Woodruff alligators (P = 0.0396). In contrast to wild-caught animals, area of the Malpighian bodies did not differ by lake in the captive-raised female alligators (P = 0.066). The enlarged thymic cortex suggests a change in T-lymphocyte maturation within the thymus of alligators from a contaminated environment, Lake Apopka. The results point to alterations in the histology of the thymus and spleen. Further studies are required to examine the functional significance of these observations.

Epigenetic programming alterations in alligators from environmentally contaminated lakes

“…The contamination of these lakes has previously been documented with a variety of toxicants identified in Table 1. Previously the health impacts on the alligators in the contaminated AP and MI lakes in comparison with the non-contaminated WO lake have been reported (Guillette et al, 1994; Gunderson et al, 2001; Milnes et al, 2005, 2008; Moore et al, 2010; Rooney et al, 2003), Table 1. The high contamination levels in the Superfund AP and MI sites have been reported (Guillette et al, 1994; Horai et al, 2014) in comparison to the negligible contamination in the WO site.…”

“…A number of previous studies have demonstrated that alligators from lakes containing a variety of environmental toxicants have significant developmental and reproductive impairments when compared to those animals living in relatively pristine environments (Hamlin and Guillette, 2010; Orlando and Guillette, 2007). A well established example results from comparisons between two central Florida, USA lakes: Lake Apopka (AP) is characterized by moderate levels of agricultural and industrial contaminants, many of which are known endocrine disrupting chemicals (EDCs), and Lake Woodruff (WO) serves as reference site as it is geographically proximate but has remained relatively pristine and undeveloped (Guillette et al, 1994; Gunderson et al, 2001; Milnes et al, 2005, 2008; Moore et al, 2010; Rooney et al, 2003), Fig. 1.…”

Effects of Organochlorine Contaminants on Loggerhead Sea Turtle Immunity: Comparison of a Correlative Field Study andIn VitroExposure Experiments

“…Although traditional thought would have expected immune suppression (Harper et al 1993; Silkworth et al 1984), enhanced lymphocyte proliferation and PHA skin responses have been observed after OC exposure in several controlled laboratory studies with wildlife species (Peden-Adams 1999; Segre et al 2002; Smits et al 2002; Wu et al 1999). Environmental studies with free-ranging wildlife and epidemiologic studies with humans have also shown significant, positive relationships between lymphocyte proliferation and OC exposure (Croisant and Grasman 2002; Lü and Wu 1985; Peden-Adams et al 1996; Rooney et al 2003). The immunoenhancement noted in these previous laboratory and environmental studies support the conclusions that OCs may enhance certain responses of loggerhead turtle immune cells and that lymphocyte proliferation may indeed be a useful biomarker of exposure to OCs.…”

Abnormal bone composition in female juvenile American alligators from a pesticide-polluted lake (Lake Apopka, Florida).

“…EDCs can affect different hormonal systems in vertebrates, including alligators, such as a) thyroid hormones, which are critical for growth, differentiation, and metabolic regulation Hewitt et al 2002); and b) sex steroids, which regulate reproductive functions but have effects throughout the organism (Guillette et al 1999b;Iguchi et al 2001). We have previously shown that alligators living in contaminated environments have a number of abnormalities in the reproductive, endocrine, and immune systems, including altered plasma sex steroid concentrations Rooney et al 2003).…”

“…Recent studies have extended this work to other systems influenced by sex and stress steroids, such as the immune system. We have observed alterations in immune tissue histology and immune cell function for animals from Lake Apopka (Rooney 1998;Rooney et al 2003).…”