Pathogen-mediated natural and manipulated population collapse in an invasive social insect

Abstract

SignificanceInvasive social insects are among the most damaging of invasive organisms and have proved universally intractable to biological control. Despite this, populations of some invasive social insects collapse from unknown causes. We report long-term studies demonstrating that infection by a microsporidian pathogen causes populations of a globally significant invasive ant to collapse to local extinction, providing a mechanistic understanding of a pervasive phenomenon in biological invasions: the collapse of established populations from endogenous factors. We apply this knowledge and successfully eliminate two large, introduced populations of these ants. More broadly, microsporidian pathogens should be evaluated for control of other supercolonial invasive social insects. Diagnosing the cause of unanticipated population collapse in invasive organisms can lead to applied solutions.

Keywords: Nylanderia fulva; biological control; invasive ant; microsporidia; natural enemy.

Fig. 1.

Map of study sites. Sites are categorized by the type of data collected. Longitudinal tracking sites: N. fulva abundance and infection status tracked over multiple years. Infection testing sites: tests from a single sampling event of N. fulva for the microsporidian pathogen M. nylanderiae. Experimental inoculation: sites where M. nylanderiae was intentionally introduced into the N. fulva population. See SI Appendix, Fig. S3 for South American sampling locations.

Fig. 2.

Infected tawny crazy ant population decline. Data from N. fulva local populations infected with M. nylanderiae where time of pathogen colonization is known or could be estimated. Data at 0 on the x-axis are from time points prior to M. nylanderiae presence. Bars provide SDs. Inset map: Plus symbols indicate excluded infected sites where the date of pathogen colonization is unknown. Tawny crazy ants also declined at these sites. Numbers identify sites in SI Appendix, Table S1. Line provides overall decline trend [abundance (log): n = 39, R² = 0.60, P < 0.0001] (SI Appendix, Table S2).

Fig. 3.

Relationships between site-level disease states and host abundance. Each point presents a site average for a sampling interval. (A) Relationships between site-level disease prevalence of M. nylanderiae infection and incidence disease burden: the average disease burden of N. fulva workers from infected nests. Only nonzero data are fitted (linear regression: disease burden [log]: n = 28, R² = 0.37, P < 0.0006) (SI Appendix, Table S2). (B) Average disease burden of workers from all nests and the local abundance of N. fulva [linear regression: abundance (log): n = 52, R² = 0.37, P < 0.0001] (SI Appendix, Table S2). Bars provide SDs.

Fig. 4.

Rise in disease intensity over elapsed time since inoculation. Dashed lines indicate inoculation day. Bars display SDs. For curve fits, see SI Appendix, Table S3. (A) Pathogen prevalence: fraction of nests infected with M. nylanderiae. (B) Incidence disease burden: average disease burden (spores per ant) for all nests testing positive for infection. Zero values indicating no positive nests are not fitted.

Fig. 5.

Tawny crazy ant abundance over time. (A) N. fulva abundance (average number of N. fulva workers per pitfall trap) at inoculation sites across time since inoculation. Dashed lines indicate inoculation day. For curve fits, see SI Appendix, Table S3. (B) Abundance of N. fulva at uninfected sites across elapsed population monitoring time. Numbers identify sites in SI Appendix, Table S1. Bars display SDs.

Fig. 6.

Brood production of tawny crazy ant colony fragments. Brood production for all colony fragments regardless of infection status by month of year. Months divided into northern hemisphere seasons by vertical dashed lines. Bars provide SE. Inset pie diagrams display the brood composition of N. fulva colony fragments infected with M. nylanderiae (n = 68) and uninfected (n = 79) by season of collection.

Fig. 7.

The seasonally dependent fate of laboratory-held tawny crazy ant nest fragments. Failure is defined as decline to 25% of original nest fragment size. Uninfected nests did not differ in their decline trajectory based upon season of collection and are displayed as a group (Kaplan-Meier survival time, log-rank: X² = 0.61, n = 61, P < 0.43). Infected fragments decline faster if collected in fall-winter than in spring-summer (Kaplan-Meier survival time, log-rank: X² = 15.5, n = 41, P < 0.0001).