Importation of exotic ticks and tick-borne spotted fever group rickettsiae into the United States by migrating songbirds

Abstract

Birds are capable of carrying ticks and, consequently, tick-transmitted microorganisms over long distances and across geographical barriers such as oceans and deserts. Ticks are hosts for several species of spotted fever group rickettsiae (SFGR), which can be transmitted to vertebrates during blood meals. In this study, the prevalence of this group of rickettsiae was examined in ticks infesting migratory songbirds by using polymerase chain reaction (PCR). During the 2009 and 2010 spring migration season, 2064 northward-migrating passerine songbirds were examined for ticks at Johnson Bayou, Louisiana. A total of 91 ticks was removed from 35 individual songbirds for tick species identification and spotted fever group rickettsia detection. Ticks were identified as Haemaphysalis juxtakochi (n=38, 42%), Amblyomma longirostre (n=22, 24%), Amblyomma nodosum (n=17, 19%), Amblyomma calcaratum (n=11, 12%), Amblyomma maculatum (n=2, 2%), and Haemaphysalis leporispalustris (n=1, 1%) by comparing their 12S rDNA gene sequence to homologous sequences in GenBank. Most of the identified ticks were exotic species originating outside of the United States. The phylogenetic analysis of the 71 ompA gene sequences of the rickettsial strains detected in the ticks revealed the occurrence of 6 distinct rickettsial genotypes. Two genotypes (corresponding to a total of 28 samples) were included in the Candidatus Rickettsia amblyommii clade (less than 1% divergence), 2 of them (corresponding to a total of 14 samples) clustered with Rickettsia sp. “Argentina” with less than 0.2% sequence divergence, and 2 of them (corresponding to a total of 27 samples), although closely related to the R. parkeri–R. africae lineage (2.50–3.41% divergence), exhibited sufficient genetic divergence from its members to possibly constitute a new rickettsial genotype. Overall, there does not seem to be a specific relationship between exotic tick species, the rickettsiae they harbor, or the reservoir competence of the corresponding bird species.

Avian Migrants Facilitate Invasions of Neotropical Ticks and Tick-Borne Pathogens into the United States

“…Based on mitochondrial 12S rDNA and ITS2 sequences, we identified seven different Amblyomma species and a single Ixodes species (Table 1). Due to similar appearances and identical DNA sequences at the loci we examined, we could not differentiate between Amblyomma maculatum and Amblyomma triste, as was the case in a recent study of bird ticks (7). The single Ixodes tick shared 96% sequence homology with Ixodes minor recovered from a bird in Costa Rica (GenBank accession no.…”

“…Additionally, we estimated a range for annual neotropical tick propagule pressure using the minimum and maximum values from species-specific infestation frequency across infested bird species. Although our data come from only a single field site, we assume migrants captured at this site are representative of neotropical migrants entering the United States, because (i) migratory birds that stop over along the northern coast of the Gulf of Mexico during spring breed across North American latitudes (40,41), and (ii) the only other study to systematically examine northbound spring migrants arriving in the United States found a remarkably similar exotic tick infestation prevalence (7).…”

“…Birds are increasingly recognized for their roles as reservoirs and hosts to vectors for a suite of emerging zoonotic diseases, including West Nile virus, Lyme disease, influenza A virus, and H5N1 avian influenza virus (3,4), and they have been implicated in the range expansion and introduction of new pathogens. Additionally, migratory birds have the potential to disperse ectoparasites and their associated pathogens over long distances (5)(6)(7).…”

“…If such transcontinental movements coincide with attachment and feeding by ticks, avian migration can facilitate the rapid movement of ticks. In the only previous study to systematically examine northbound spring migrants for ticks immediately upon entry into the United States, Mukherjee et al (7) found that 3% of songbirds hosted a tick, some of which were infected with spotted fever group Rickettsia species. Further, Central and South American Amblyomma spe-cies have been detected on northward-migrating birds as far north as Chicago, IL, and Canada (5,6,17,18).…”

Ticks (Acari: Ixodidae) as ectoparasites of Brazilian wild birds and their association with rickettsial diseases

“…Migratory birds in particular have received much attention as they can transport potentially infected ticks across large areas and may account for the origin of some new foci of diseases (ANDERSON et al, 1986;OLSEN et al, 1995a;KLICH et al, 1996;SMITH et al, 1996;RAND et al, 1998;KINSEY et al, 2000;SCOTT et al, 2001SCOTT et al, , 2010SCOTT et al, , 2012JONGEJAN et al, 2004;MORSHED et al, 2005;DUBSKA et al, 2009;ELFVING et al, 2010;HILDEBRANDT et al, 2010;KJELLAND et al, 2010;HASLE et al, 2011;HASLE, 2013;MOVILA et al, 2011;GELLER et al, 2013;CAPLIGINA et al, 2014), even introducing them to different continents (OLSEN et al, 1995b;MUKHERJEE et al, 2014;. Although the role of birds as hosts and disseminators of ticks has received much attention over the past several years, there is a lack of studies in South America, including Brazil.…”