Relationships of salinity, relative humidity, mud flat fiddler crabs, ants, and sea ox-eye daisy with ixodid distribution and egg survival on the South Texas coastal plains

Authors: Showler, Allan; Osbrink, Weste; ABRIGO, VERONICA - Non ARS Employee; PHILLIPS, PAMELA - Former ARS Employee

Submitted to: Environmental Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/31/2019
Publication Date: 6/20/2019
Citation: Showler, A., Osbrink, W.L., Abrigo, V., Phillips, P. 2019. Relationships of salinity, relative humidity, mud flat fiddler crabs, ants, and sea ox-eye daisy with ixodid distribution and egg survival on the South Texas coastal plains. Environmental Entomology. 48(3):733-746. https://doi.org/10.1093/ee/nvz034.
DOI: https://doi.org/10.1093/ee/nvz034

Interpretive Summary: The South Texas coastal plains are mostly mesquite-dominated thorn scrub in Cameron and Willacy counties from the Mexico border to cattle ranches in and north of Willacy County. The coastal plains constitute a corridor for wild tick hosts, much of it protected by wildlife refuges, and it is part of a permanent cattle fever tick quarantine zone designed to exclude the cattle fever tick and the southern cattle fever tick (SCFT), and the disease babesiosis that they transmit, from Texas. In 2016 the southern cattle fever tick was found Approximately 175 km inside Texas far north of the quarantine zone. At least six other ixodid tick species, each of which vectors multiple pathogens of humans and other animals, inhabit the South Texas coastal plains. While many animal tick hosts inhabit the region, two of the most important (mainly for hosting SCFT) are exotic nilgai antelope and native white-tailed deer. Occasional wind tides and infrequent storm surges inundate large coastal plain areas with hypersaline water from the Lower Laguna Madre and created extensive areas of highly saline soil. Although salt water does not necessarily kill the mobile stages of ixodid ticks, brief exposure to marine and hypersaline water are highly lethal to lone star tick and SCFT eggs, indicating that wind tides and storm surges eliminate ixodid eggs in flooded areas. Saline soil itself is not necessarily toxic to ixodid eggs. Dry saline and low-salinity soils in laboratory assays were associated with desiccation of the tick eggs while saline moistened and moistened low-salinity soils favored hatching; elevated RH was associated with relatively high hatches regardless of whether soil was dry and saline. Large year-round populations of mud flat fiddler crabs occur on saline soil and they consume approximately 80% of lone star tick egg masses overnight (most ixodid tick eggs hatch after >20 d). Areas of saline soil extend at least 34.5 km inland from the Lower Laguna Madre and all of these areas are inhabited by large populations of the crab. Saline soils are strongly associated with the sea ox eye plant which has a distinctive gray-green color that enabled GIS-based mapping. At least 24.4% of the South Texas coastal plains wildlife corridor is dominated by sea ox eye. Tick sampling showed that numbers are negligible in sea ox eye stands in saline areas and relatively abundant on mixed thorn scrub vegetation typical of low-salinity soil. Hence, tick distribution on the South Texas coastal plains is governed by salinity both from the ovicidal action of salt water, desiccation, and from egg predation by the fiddler crab. Although predatory ants, especially the red imported fire ant, have been reported to cause ixodid tick population suppression, we found that predatory ant species common to saline and low-salinity soil habitats do not attack lone star tick egg masses. We suggest that ants are a weak mortality factor against ixodid tick eggs and that, where it exists, the mud flat fiddler crab is a decisive mortality factor. Overlaid on the mosaic landscape of salinity and predator mortality factors is an abundance of nilgai, white-tailed deer, and other ixodid tick hosts that continually move about overlapping home ranges, creating a mobile system that can pick up and deposit ticks in tick-favorable low-salinity habitats and in antagonistic saline habitats alike. Our findings present a unique and complex ecology of ixodid tick species.

Technical Abstract: The humid, flat coastal plains of deep South Texas along the mainland side of the Lower Laguna Madre is mostly comprised of subtropical, mesquite-dominated thorn scrub in Cameron and Willacy counties from the border with Mexico to large cattle ranches that extend northward from Willacy County. The South Texas coastal plains region is a corridor for wild hosts of ticks, much of its area protected as wildlife refuges, and it is part of a permanent cattle fever tick quarantine zone designed to exclude the two cattle fever tick species, Rhipicephalus (Boophilus) microplus (Canestrini) and R. (Boophilus) annulatus (Say), and the causal agents of cattle babesiosis that they transmit, from Texas. In 2016, however, the southern cattle fever tick, R. microplus, was found as far north as Live Oak County, approximately 175 km inside Texas and far north of the permanent quarantine zone. At least six other ixodid tick species, each of which vectors multiple pathogens of medical and veterinary importance, inhabit the South Texas coastal plains. While many mammalian and avian ixodid tick hosts live in the region, two of the most important (mainly for hosting R. microplus) are the exotic nilgai antelope, Bosephalus tragocamelus Pallas, and the indigenous white-tailed deer, Odocoilus virginianus (Zimmerman). Occasional wind tides and infrequent storm surges that inundate large coastal plain areas with hypersaline water from the Lower Laguna Madre have created extensive areas of highly saline soil. We determined that, although salt water does not necessarily kill ixodid tick larvae, nymphs, and adults, brief exposure to marine and hypersaline water are highly lethal to lone star tick, Amblyomma americanum (L.), and R. microplus eggs, indicating that wind tides and storm surges will eliminate ixodid eggs in flooded areas. We found that saline soil itself is not necessarily toxic to ixodid eggs. Dry saline and low-salinity soils in laboratory assays were associated with desiccation of the tick eggs while saline moistened and low-salinity soils favored hatching; elevated RH was associated with relatively high hatches regardless of whether soil was dry and saline. Large year-round populations of mud flat fiddler crabs, Uca rapax (Smith), occur on saline soil and they readily consume A. americanum eggs, consistently removing approximately 80% of egg masses overnight (most ixodid tick eggs hatch after >20 d). Areas of saline soil extend at least 34.5 km inland from the Lower Laguna Madre and all of these areas are inhabited by large populations of U. rapax. The saline areas are strongly associated with the sea ox eye, Borrichia frutescens (L.) DC, plant which has a distinctive gray-green color that enabled GIS-based mapping. We determined that at least 24.4% of the South Texas coastal plains wildlife corridor is dominated by B. frutescens. Ixodid tick sampling showed that tick numbers are negligible on B. frutescens stands in saline areas and relatively abundant on mixed thorn scrub vegetation typical of low-salinity soil. Hence, ixodid tick distribution on the South Texas coastal plains is governed by salinity both from the ovicidal action of salt water and from egg predation by U. rapax. Although predatory ants, especially the aggressive red imported fire ant, Solenopsis invicta (Buren), have been reported to cause ixodid tick population suppression, we found that predatory ant species common to saline and low-salinity soil habitats do not attack A. americanum egg masses (evidence for allomone-based protection against ants is discussed). We suggest that ants are a weak mortality factor against ixodid tick eggs and that, where it exists, U. rapax is a strong mortality factor. Overlaid on the mosaic landscape of salinity and predator mortality factors is an abundance of nilgai, white-tailed deer, and other ixodid ticks hosts that continually move about