Background
Selenium (Se) can readily be transferred from one organism to another by trophic interactions and maternal transfer. Vertebrates primarily accumulate Se by digesting Se-enriched food and incorporating constituent organo-selenium compounds (e.g., seleno-amino acids), or Se from these compounds, into their own biomolecules. Following Se accumulation, female oviparous vertebrates (fish and birds) readily transfer Se to developing offspring, most likely via incorporation of seleno-amino acids into egg yolk proteins. Upon being transferred excessively from dietary or maternal sources, some seleno-amino acids (e.g., selenocystine) can be cytotoxic due to oxidative damage. It is also theorized that substitution of other seleno-amino acids (e.g., seleno-methionine) into proteins may alter their structure, and therefore function, perhaps causing Se toxicity and teratogenesis.

Brown house snake

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Brown house snake (Lamprophis fuliginosus).

Dietary and maternal transfer of Se has been well-studied in birds and fish, but little is known about the transfer and effects of Se in reptiles or amphibians. A limited number of field studies indicate that reptiles in Se-contaminated habitats accumulate high tissue burdens of Se. Although laboratory studies on reptile accumulation of Se are generally lacking, a suite of recent studies confirmed that trophic transfer is a significant route of exposure to Se (and other trace elements) for viviparous snakes. Maternal transfer of Se has been documented in field-collected turtles, but to our knowledge, no controlled laboratory study has examined accumulation and subsequent maternal transfer of Se (or any trace element) in a reptile or amphibian.

We recently conducted an experiment to study the trophic and maternal transfer of Se in a reptile under captive conditions, enabling us to control the dose, chemical species, duration, and route of Se exposure. We exposed female brown house snakes, Lamprophis fuliginosus, to 10 and 20 µg/g Se by injecting seleno-D,L-methionine into their prey items and compared the snakes to individuals receiving background levels of ~ 1 µg/g dietary Se. Snakes were on their respective diets for 10 months and we measured Se accumulation as well as survival, food consumption, growth, and body condition. In addition, we paired females with untreated males and quantified the number of females that reproduced, reproductive output of each female (number of clutches, total number of eggs, and total mass of combined clutches), and maternal transfer of Se to eggs.

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10-month growth rate
Why House Snakes?
Lamprophis fuliginosus is one of the most common terrestrial Colubrid snakes in southern Africa, with a range extending across the entire sub-Saharan continent. Adult L. fuliginosus prey upon a wide variety of organisms including lizards, birds, and even bats, but the bulk of their diet consists of rodents.

The ability of L. fuliginosus to attain reproductive size quickly and to reproduce frequently makes this species a logical starting point for controlled toxicological studies on snakes. The species is oviparous, laying clutches of up to 16 eggs, but usually fewer. In the laboratory, reproduction requires no stimulatory environmental cues (e.g., change in photoperiod or temperature) and occurs year-round. Under optimal conditions in captivity, female L. fuliginosus can attain reproductive size within 10 months and produce eggs as frequently as 8 times a year. In contrast, most North American Colubrid species require at least two years to reach reproductive maturity and will only produce 1-2 clutches per year.

Typical growth over 10 months: hatchling vs. adult brown house snake.
fig. 1

Key Findings
Our study demonstrated that snakes accumulate Se from ingesting seleniferous prey, ultimately resulting in maternal transfer of potentially toxic quantities of Se to their offspring. Few previous studies have experimentally examined trophic uptake of contaminants in squamate reptiles, and our study is the first to document maternal transfer of an environmental contaminant in a reptile under controlled laboratory conditions.

Snakes exposed to excessive Se accumulated significant concentrations of Se in kidney, liver, and ovarian tissue, but accumulation had no effect on female survival, food consumption, growth, or body condition. On average, fewer females exposed to excessive Se reproduced compared to females exposed to 1 µg/g Se (67 % vs. 91%, respectively), but the reduction in reproductive activity was not statistically significant. Total reproductive output of females did not differ among the three dietary treatments. However, snakes exposed to 10 and 20 µg/g Se transferred significant concentrations of Se to their eggs. In the 20 µg/g treatment, maternal transfer resulted in Se concentrations in eggs that surpassed all suggested reproductive toxicity thresholds for birds and fish. Further studies are needed to more rigorously determine whether maternal transfer of Se in this snake species affects the viability of developing embryos or the health of offspring.

Mean trace element accumulation in organs (µg/g dry mass) of female brown house snakes (Lamprophis fuliginosus) fed rodents containing different dietary concentrations of Se (< 1, 10, and 20 µg/g dry mass) for 10 months. Error bars represent ± 1 SE.
fig. 2
Table 1. Reproductive traits of female L. fuliginosus fed diets containing varying levels of Se (1-20 µg/g dry mass). With the exception of parameters expressed on a percentage basis, all data are presented as mean 1 ± SE.
 
   Treatment
 Reproductive Parameter
 1 ug/g
10 ug/g
20 ug/g
 % Reproductive females
91
60
73
 Reproductive Output/Female

xxTotal # clutches

1.18 ± 0.18
0.90 ± 0.28
1.18 ± 0.26

xxTotal # eggs

7.55 ± 2.77
3.00 ± 1.07
5.18 ± 1.71

xxMass of combined clutches (g)

51.04 ± 12.99
31.76 ± 11.16
42.62 ± 11.40
Individual Clutch Characteristics:

xx# Eggs/clutch

6.38 ± 1.22
3.33 ± 0.41
4.38 ± 0.67

xxClutch mass (g)

43.18 ± 4.69
35.29 ± 3.59
36.07 ± 3.83
Egg Characteristics:

xxEgg length (mm)

37.68 ± 1.69
57.69 ± 2.98
47.10 ± 1.85

xxEgg mass (g)

6.76 ± 0.35
10.59 ± 0.84
8.23 ± 0.35

xx% Viable at oviposition

60
0
59

xx% Viable that hatched

76
N/A
76

xxSe content (ug/g dry mass)

0.92 ± 0.02
12.03 ± 0.33
22.65 ± 0.49

xxxxxSe content of viable eggss

0.88 ± 0.04
N/A
22.57 ± 1.00

xxxxxSe content of inviable eggs

0.94 ± 0.03
12.03 ± 0.33
22.70 ± 0.55

Change in mean mass and snout-vent length of female brown house snakes (Lamprophis fuliginosus) fed rodents containing different dietary concentrations of Se (< 1, 10, and 20 µg/g dry mass) over the 6-month growth phase of the study. Error bars represent ± 1 SE.

fig. 3
Table 2. Characteristics of hatchling L. fuliginosus from mothers fed diets containing 1 or 20 µg/g (dry mass) selenium. No hatchling characteristics are presented for the 10 µg/g dietary treatment due to 100% inviability of eggs at oviposition for that treatment (see Table 1). SVL, Mass, and Se content are presented as Mean 1 ± SE.
 
Treatment
Hatchling Characteristic
1 µg/g
20 µg/g

SVL (cm)

20.32 ± 0.16
21.82 ± 0.40

Mass (g)

4.30 ± 0.09
5.55 ± 0.18

Sex Ratio (M/F)

16/16
13/8

Se Content (ppm dry mass)

0.98 ± 0.02
24.25 ± 0.49
Concentrations of Se in individual eggs resulting from maternal transfer from female snakes (Lamprophis fuliginosus) ingesting rodents containing different dietary concentrations of Se (< 1, 10, and 20 µg/g dry mass). Horizontal lines with corresponding letters represent toxic effects thresholds for reproductive toxicity presented by A) Fairbrother et al., 1999, B) Heinz, 1996, C) Lemly, 1996, D) Skorupa, 1998, and E) Skorupa and Ohlendorf, 1991. A total of 116 eggs are presented (N = 51, 30, and 36 eggs in the 1, 10, and 20 µg/g Se treatments, respectively).

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