Spatial Variation and Survival of Salmonella enterica Subspecies in a Population of Australian Sleepy Lizards (Tiliqua rugosa)

Abstract

The life cycles of many enteric bacterial species require a transition between two very distinct environments. Their primary habitat is the gastrointestinal tract of the host, while their secondary habitat, during transmission from one host to another, consists of environments external to the host, such as soil, water, and sediments. Consequently, both host and environmental factors shape the genetic structure of enteric bacterial populations. This study examined the distribution of four Salmonella enterica subspecies in a population of sleepy lizards, Tiliqua rugosa, in a semiarid region of South Australia. The lizards living within the 1,920-m by 720-m study site were radio tracked, and their enteric bacteria were sampled at regular intervals throughout their active seasons in the years 2001, 2002, and 2006. Four of the six subspecies of S. enterica were present in this population and were nonrandomly distributed among the lizards. In particular, S. enterica subsp. diarizonae was restricted to lizards living in the most shaded parts of the study site with an overstorey of Casuarina trees. Experiments undertaken to investigate the survival of S. enterica cells under seminatural conditions revealed that cell survival decreased with increased exposure to elevated temperatures and UV light. Among the three S. enterica subspecies tested, S. enterica subsp. diarizonae consistently had an average expected life span that was shorter than that observed for the other two subspecies. There was no indication in the data that there was any competitive dominance hierarchy among the S. enterica subspecies within individual hosts. Thus, the nonrandom distribution of S. enterica subspecies in this population of lizards appears to be driven by their different survival characteristics in the external environment.

FIG 1

Changes in the proportions of sleepy lizards in which S. enterica was detected over the course of the 2006 field season at Mt. Mary, South Australia.

FIG 2

S. enterica subspecies carriage in the sleepy lizard population. ▲, average number of subspecies present per lizard; ●, cumulative number of lizards, out of a total of 28 lizards, that harbored two or more subspecies over the season.

FIG 3

Temporal changes in the S. enterica subspecies detected in each T. rugosa individual over the active season of 2006. On the left are the lizard numbers, while columns 1 to 15 represent the sampling occasions in chronological order from left to right. Each colored box represents a sample. White, no S. enterica; yellow, S. enterica subsp. enterica; blue, S. enterica subsp. diarizonae; red, S. enterica subsp. salamae; black, S. enterica subsp. houtenae; gray, lizard not sampled. The amounts of color in each sampling box represent the relative frequency of each of the subspecies found in the sample.

FIG 4

Distribution of S. enterica subspecies in the Mt. Mary study site in the years 2001, 2002, and 2006. In each diagram, each point corresponds to the location of a lizard harboring a particular subspecies when it was sampled. The spatial locations of each subspecies detected in a lizard were fitted using a nonparametric bivariate density algorithm. This analysis identifies the spatial locations corresponding to the region where a particular subspecies was most likely to be detected in a lizard. The red and yellow contours correspond to a high probability of detecting a particular subspecies, while the green and blue contours correspond to the areas where a particular subspecies was less likely to be detected in a lizard. D,S. enterica subsp. diarizonae; E, S. enterica subsp. enterica; S, S. enterica subsp. salamae.