Aspects of spatial and habitat ecology of multiple Anopheles species (Diptera: Culicidae): malaria vectors in the highlands and foothills of Ecuador

The resurgence of malaria in highland regions of Africa, Oceania and recently in South America underlines the importance of the study of the ecology of highland mosquito vectors of malaria. Since the incidence of malaria is limited by the distribution of its vectors, the purpose of this PhD thesis was to examine aspects of the ecology of Anopheles mosquitoes in the Andes of Ecuador, South America. A historical literature and archival data review (Chapter 2) indicated that Anopheles pseudopunctipennis transmitted malaria in highland valleys of Ecuador prior to 1950, although it was eliminated through habitat removal and the use of chemical insecticides. Other anopheline species were previously limited to low-altitude regions, except in a few unconfirmed cases. A thorough larval collection effort (n=438 attempted collection sites) in all road-accessible parts of Ecuador except for the lowland Amazon basin was undertaken between 2008 - 2010 (Chapter 3). Larvae were identified morphologically and using molecular techniques (mitochondrial COl gene), and distribution maps indicated that all five species collected (Anopheles albimanus, An. pseudopunctipennis, Anopheles punctimacula, Anopheles oswaldoi s.l. and Anopheles eiseni) were more widespread throughout highland regions than previously recorded during the 1940s, with higher maximum altitudes for all except An. pseudopunctipennis (1541 m, 1930 m, 1906 m, 1233 m and 1873 m, respectively). During larval collections, to characterize species-specific larval habitat, a variety of abiotic and biotic habitat parameters were measured and compared between species-present and species-absent sites using chi-square tests and stepwise binary logistic regression analyses (Chapter 4). An. albimanus was significantly associated with permanent pools with sand substrates and An. pseudopunctipennis with gravel and boulder substrates. Both species were significantly associated with floating cyanobacterial mats and warmer temperatures, which may limit their presence in cooler highland regions. Anopheles punctimacula was collected more often than expected from algae-free, shaded pools with higher-than-average calculated dissolved oxygen. Anopheles oswaldoi s.l., the species occurring on the Amazonian side of the Andes, was associated with permanent, anthropogenic habitats such as roadside ditches and ponds. To address the hypothesis that human land use change is responsible for the emergence of multiple highland Anopheles species by creating larval habitat, common land uses in the western Andes were surveyed for standing water and potential larval habitat suitability (Chapter 5). Rivers and road edges provided large amounts of potentially suitable anopheline habitat in the western Andes, while cattle pasture also created potentially suitable habitat in irrigation canals and watering ponds. Other common land uses surveyed (banana farms, sugarcane plantations, mixed tree plantations, and empty lots) were usually established on steep slopes and had very little standing water present. Using distribution and larval habitat data, a GIS-based larval habitat distribution model for the common western species was constructed in ArcGIS v.l 0 (ESRI 2010) using derived data layers from field measurements and other sources (Chapter 6). The additive model predicted 76.4 - 97.9% of the field-observed collection localities of An. albimanus, An. pseudopunctipennis and An. punctimacula, although it could not accurately distinguish between species-absent and speciespresent sites due to its coarse scale. The model predicted distributional expansion and/or shift of one or more anopheline species into the following highland valleys with climate warming: Mira/Chota, Imbabura province, Tumbaco, Pichincha province, Pallatanga and Sibambe, Chimborazo province, and Yungilla, Azuay province. These valleys may serve as targeted sites of future monitoring to prevent highland epidemics of malaria. The human perceptions of malaria and mosquitoes in relation to land management practices were assessed through an interview-based survey (n=262) in both highlands and lowlands, of male and female land owners and managers of five property types (Chapter 7). Although respondents had a strong understanding of where the disease occurs in their own country and of the basic relationship among standing water, mosquitoes and malaria, about half of respondents in potential risk areas denied the current possibility of malaria infection on their own property. As well, about half of respondents with potential anopheline larval habitat did not report its presence, likely due to a highly specific definition of suitable mosquito habitat. Most respondents who are considered at risk of malaria currently use at least one type of mosquito bite prevention, most commonly bed nets. In conclusion, this interdisciplinary thesis examines the occurrence of Anopheles species in the lowland transition area and highlands in Ecuador, from a historic, geographic, ecological and sociological perspective.

Charles Larned letter, April 3, 1813.

Charles Larned (1791-1834) was a lawyer and American military officer who served during the War of 1812. He was the son of Simon Larned (1753-1817), who served as a captain in the Revolutionary War and was a member of the United States Congress from Massachusetts from 1804-1805. Charles studied law in the office of Henry Clay in Kentucky, and was dining with a group of prominent citizens when word was received that General William Henry Harrison could soon be overpowered by General Henry Proctor. Colonel Owen, a member of the group, organized a regiment to reinforce Harrison’s troops. Larned became a member and subsequently survived the River Raisin Massacre and was later present at the Battle of the Thames. He was also part of a group of men who learned of General William Hull’s plan to surrender Detroit to the British and planned to overtake him should this occur. However, the plan failed, Hull did surrender and the men became prisoners of the British. After the war, Larned became a lawyer, and served as Attorney General of Michigan Territory during the Black Hawk War. During the cholera epidemic of 1834, he worked tirelessly to assist others, but was stricken with the disease and died. Letter Transcription: Pittsfield, April 8, 1813 I think that by this time my dear Charles you will allow I have some reason to give you a gentle reprimand for breach of duty—but I will not censure you upon suspicion maybe you have substantial reasons—at any rate one cannot very graciously reproach the other for negligence I for one am healthy as ham & that we have so seldom exchanged letters during your absence & on my honor promise to be a better girl in future—but the truth is my Dear Charles I am secretary for the Family—Mama you know never writes & James but seldom & they are all dispersed in different directions, consequently I have many calls upon my time—this to be sure is a pleasant duty & I urge it only as a slight palliation for my remissness if you should consider it as such—now I have finished my preface—I will try to be more interesting & doubtless I succeed. Our dear Father we hope & trust is now in Green Bush, where he will probably remain a month perhaps & from thence he expects to go to Sacket’s harbor—at which place you know our troops are fast collecting-- We shall hope to see him either here or there before he goes. Brother George I believe is [still] at Plattsburgh but expects soon to be removed to some other military part perhaps with Papa (I hope so at least). We have just got letters from Brothers Sylvester & Joseph at Middlebury—they are in good health. Mama has for some weeks been afflicted with an inflammation in her eyes but seems now to be convalescing. Sister Martha has been somewhat unwell for a few weeks but is now tolerably recovered. James & myself are both in our usual good health & at this time seated by the same stand, one reading, the other writing. Thus my Dear Charles have I given you an abstract history of our Family—but here indeed is a wonderful omission; not a word about Miss Harriet Hunt, who in truth ought to have been noted first but the last she’s not the least in my memory. She is much grown since you saw her, but does not speak as fluently as we could wish—a few word she can say. Probably before this you have been informed of the great loss your friend Sherrill has sustained in the death of his mother—also of the revolution that has taken place in Hackbridge as it respects the religion & morality of the place that more than one hundred on the plain have become religious converts & c—indeed I am at a loss what to say that will afford your pleasure—a narrative at this time must be gloomy indeed. The distressing situation of our country at this time would make almost any recital melancholy. The prevailing epidemic has swept off many of your acquaintance no doubt. Mrs. Dewey of Williamstown, the sister of Mrs. Danforth, has left a Husband, Children & many Friends sincerely to lament her loss—some few have died in our village, but we have escaped astonishingly –it has raged in every town about us--If we are unwilling to acknowledge a God in his mercies. I fear she shall be compelled to do it in the awfulness of his judgments.--------I am much [pleased] with our new neighbors the Parsons Wife & a Miss Woodward her cousin is a fine girl, I think, Mrs. Allen has not a handsome face but something in her manner that interests one her person I think the handsomest I ever saw & the Parson seems well pleased with his selection—Mrs. Ripley is with them this winter & will probably remain thro the summer—Her husband at [Sackett’s Harbor] little or no alteration is apparent since her marriage—she seems as gay & fond of company as ever.-------Mrs. [McKnight] it is expected will commence housekeeping in about three weeks in the house formerly occupied by Mr…. [Report] says that Mr. Goodman & Clarissa Weller are soon to be married & many other things that I must omit to mention for Mama wants a… PS reserved--now my Dear Charles remember you are considerably… & I am confident you have as much leisure as I have –… be ceremonious but write whenever I find time not & I beg… the same – I tell James I shall not send his love for he must write himself. I shall anxiously expect you to write & do not disappoint your affectionate, sister--H One word my Dear Charles from your affectionate Mother who longs to see Her Dear son Charles—but being deprived of that rich blessing at present—begs Him so to conduct that she may hope for it ere long—do you search the Scriptures and keep the Sabbath holy unto the Lord—and all the sacred Commandments of God—it is my ardent desire…He would protect, support and provide for your soul and body and believe me your affectionate friend and Mother. R Larned.