From Galapagos doves to passerines: Spillover of Haemoproteus multipigmentatus

Abstract

Haemoproteus (Haemoproteus) multipigmentatus, a haemosporidian parasite thought to be specific to columbiform birds, was detected in passeriform birds on Santiago Island in the Galapagos archipelago. We surveyed birds along an altitudinal gradient on the islands of Santa Cruz, Isabela and Santiago between June 2013 and July 2015. Molecular screening of 2254 individuals from 25 species of endemic and introduced birds revealed clusters of passerine birds positive for H. multipigmentatus on Santiago Island that coincide with captures of Galapagos doves at sampled sites. Of 507 individuals from 10 species of endemic passerines sampled on Santiago, 58 individuals from 6 species were found positive (11% prevalence). However, no gametocytes were found in the blood smears of positive passerines, suggesting that these species are not competent hosts for the parasite. All 31 doves captured were positive and gametocytes were found upon microscopic examination of all thin blood smears (averaging 357 gametocytes per 10,000 erythrocytes). These findings indicate parasite spillover from doves to passerines, but that passerines are possibly not competent hosts for further parasite transmission. The endemic Galapagos dove acts as a reservoir host for the introduced H. multipigmentatus, however the effect of this parasite on passerines has not been studied. We report on these findings because parasites can have large effects on individual host populations and on the ecology of a community, but may go undetected.

Louse flies of Eleonora’s falcons that also feed on their prey are evolutionary dead‐end hosts for blood parasites

“…The high prevalence and diversity of lineages found in louse flies suggest that this opportunistic feeding behavior is rather common. In addition, louse flies may be involved in the transmission of Haemoproteus parasites between distantly related species, as in the case of seabirds (i.e., frigatebirds) and passerines (Jaramillo et al, ; Santiago‐Alarcon et al, ). The alternative hypothesis, that louse flies are carried by migratory passerines, is unlikely to be the case, as this louse fly species, to the best of our knowledge, has not been recorded on any other bird species than the above‐mentioned Falco species.…”

“…A newly colonized host represents a novel habitat for the parasite, and probably has a new blood cellular and immunological profile that may hamper the ability of the parasite to invade host cells, or result in the abortive development of the parasite at the tissue stage (Olias et al, ; Valkiūnas et al, ). For example, Jaramillo et al () found that H. multipigmentatus , which is a parasite that is thought to be specific to columbiform birds (Valkiūnas et al, ), was able to infect six different species of passerines that co‐occurred with the parasite's main host, i.e., the endemic Galapagos dove. However, despite a successful spillover from introduced rock pigeons ( Columba livia ) to doves and the subsequent spillover from doves to passerines, the absence of parasite gametocytes in passerine bird blood suggests that these are not competent hosts for this Haemoproteus lineage (Jaramillo et al, ).…”

“…However, vacant niches, in the form of new vectors and hosts, are available for newly arriving generalist strategists that are capable of exploiting new opportunities, thus broadening host ranges, but also for parasites that are able to flourish in new host‐vector assemblages, which in this case would promote parasite diversification (Agosta & Klemens, ; Drovetski et al, ; Medeiros, Ellis, & Ricklefs, ; Santiago‐Alarcon, Rodríguez‐Ferraro, Parker, & Ricklefs, ). In this context, the fact that louse flies are able to move between host individuals of the same or even different species, potentially increases the probability of host switching by haemosporidians (Jaramillo, Rohrer, & Parker, ; Levin & Parker, ). This may be the case for H. multipigmentatus , in that louse flies could have facilitated parasites jumping from doves to distantly related avian hosts on oceanic islands (Jaramillo et al, ; Levin & Parker, ; Levin et al, ).…”

“…In this context, the fact that louse flies are able to move between host individuals of the same or even different species, potentially increases the probability of host switching by haemosporidians (Jaramillo, Rohrer, & Parker, 2017;Levin & Parker, 2014). This may be the case for H. multipigmentatus, in that louse flies could have facilitated parasites jumping from doves to distantly related avian hosts on oceanic islands (Jaramillo et al, 2017;Levin & Parker, 2014;Levin et al, 2011).…”

Evolutionary lability of host associations promotes phylogenetic overdispersion of co‐infecting blood parasites

“…We downloaded the ‘Hosts and Sites’ table from the MalAvi database (Bensch, Hellgren, & Pérez‐Tris, ) and filtered the dataset based on two specifications: (a) haemosporidians must have been recorded in at least 10 different host individuals, and (b) we only considered a haemosporidian species capable of infecting a host family if at least 10% of all documented infections for the parasite were found in that host family. We established these cut‐offs to increase the likelihood that we were analysing biologically meaningful host–parasite associations, as haemosporidians are known to occur as spillover infections into ‘dead‐end’ hosts (Jaramillo, Rohrer, & Parker, ; Moens et al, ), which can have a misleading effect if not removed.…”