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Keywords:

  • Rhodnius;
  • sylvatic populations;
  • ecology;
  • palm trees;
  • Trypanosoma cruzi transmission;
  • Ecuador

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Most Rhodnius species (Triatominae) are primarily associated with palm trees. They maintain enzootic Trypanosoma cruzi transmission and are responsible for human infection (causing Chagas disease) through the Neotropics. Assessing whether individual palm traits (ecological and/or botanical) may increase the risk of palm infestation by triatomines is relevant in areas where bugs invade houses flying from peridomestic palms. We developed a novel fieldwork approach with that objective, and applied it to study infestation by sylvatic Rhodnius ecuadoriensis in 110 tagua palms (Phytelephas aequatorialis). Palm infestation (23% overall) was non-randomly distributed in our sample. Palms located in anthropic landscapes were frequently infested (>27%, n = 92), whereas no bugs were collected from palms surveyed within forest remnants (n = 18; P = 0.01). The presence of abundant decaying vegetable matter (P = 0.001) and (to a lesser extent) epiphytic plants (P = 0.049) on palm crowns and stems increased the probability of infestation and was positively correlated with the apparent density of bug colonies (R2 = 0.68). A trend towards higher infestation rates in male palms (34%vs. 18%) could relate to female palm management (removal of infrutescences and vegetable debris) in areas where palm seeds are harvested. An outline of ‘risk palm ecotopes’ and environmental management-based strategies for the control of peridomestic, palm tree-living vector populations are proposed.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The logic of describing ecotope traits that favour infestation by synanthropic triatomines has been instrumental to define ‘risk households’ and thus develop rational schemes for the control of Chagas disease transmission (e.g. Cohen & Gürtler 2001 and references therein). However, it has rarely been applied to the study of sylvatic bug populations (Romaña et al. 1999; Noireau et al. 2000). With the current success of control programmes targeting domestic vectors (WHO 2002; Morel & Lazdins 2003), researchers and public health authorities are increasingly interested in understanding the ecology and behavioural trends of sylvatic bug populations. Reinfestation of insecticide-treated households by wild vectors is still common, and sylvatic bug populations actively transmit Chagas disease in wide regions of the Americas (Miles et al. 2003; Morel & Lazdins 2003).

Rhodnius species maintain enzootic Trypanosoma cruzi cycles and are responsible for human infection in parts of Central America, Venezuela, Colombia, Ecuador, Peru, Bolivia and Brazil, including the whole Amazon basin. Nearly all of these species breed in palm trees (Lent & Wygodzinsky 1979; Barrett 1991; Carcavallo et al. 1998a). They display varying patterns of habitat association, from apparently strict specialists infesting single palm species (e.g. R. brethesi) to generalists recorded from several palm genera (e.g. R. pictipes; Table 1). The biogeographical range of most Rhodnius species matches that of the palms they occupy, often in humid or seasonally dry forests (Barrett 1991). Ecological data suggesting an ancient association between Rhodnius and palms recently received further support from DNA sequence data analysis (Gaunt & Miles 2000, 2002).

Table 1. Rhodnius and palm trees in the Americas
Rhodnius speciesPalm tree habitats*Remarks
  1. * At least 13 palm genera; the widespread use of synonyms in palm taxonomy complicates the assessment at the species level.

R. brethesiLeopoldinia piassabaApparently specialized
R. colombiensisAttalea (=Maximiliana) butyracea (=macrocarpa, maracaibensis, marolepis, humboldtiana)Apparently specialized
R. dalessandroiOenocarpus (=Jessenia) polycarpaTaxonomic status dubious
R. domesticusAttalea sp.Preferentially in bromeliads and mammal nests
R. ecuadoriensisPhytelephas aequatorialis, Elaeis guineensisOne record in E. guineensis
R. nasutusCopernicia cerifera (= prunifera)Arid life zones; also bird nests
R. neglectusOrbignya maritima, Or. oleifera, Or. martiana, Acrocomia macrocarpa, Ac. sclerocarpa (=aculeata), Mauritia vinifera, M. flexuosa, A. phalerata, A. speciosa, Arecastrum romanzoffianum, Syagrus oleraceaGeneralist; also bird and mammal nests
R. neivaiCopernicia tectorum, Attalea spp.Arid environments
R. pallescensA. butyracea, Cocos nucifera, E. oleifera, O. bataua, Co. tectorumGeneralist
R. pictipesA. butyracea, A. maripa (=M. regia), A. speciosa, O. bataua, O. polycarpa, Astrocaryum urostachys, E. guineensis, Ph. tenuicaulis, Ac. sclerocarpa, Mauritia sp., Co. australis, Or. SpeciosaGeneralist; also bromeliads; wide range across the Amazon
R. prolixusA. butyracea, A. elegans, Co. tectorum, M. flexuosa, M. minor, Or. phalerata, Or. speciosa, Ac. sclerocarpa, Sabal mauritiiformis, C. nucifera, O. bataua, O. polycarpa, L. piassabaGeneralist; also in trees, bird nests, bromeliads, and mammal shelters. Sylvatic in the Orinoco basin
R. robustusA. butyracea, A. maripa, A. speciosa, O. bataua, O. bacaba, As. urostachys, E. guineensis, Ph. tenuicaulis, M. carana, Ac. sclerocarpa, Or. speciosaProbably encompassing several cryptic taxa; also in bromeliads and vertebrate nests
R. staliA. phalerataA single record

Contact between humans and palm tree-living Rhodnius populations may increase as a result of anthropogenic environmental change. Thus, selective deforestation respects peridomestic palms, and some palm species pioneer forest regrowth; therefore, palms are often abundant near human habitations in many regions (Whitlaw & Chaniotis 1978; Barrett 1991; Henderson et al. 1995; Palomeque et al. 2000). Rhodnius bugs, pre-adapted to palms and eclectic feeders (cf. Carcavallo et al. 1998b), can establish large colonies in peridomestic palms, feeding on opportunistic mammals that thrive in anthropic landscapes and take shelter in the palms (mainly opossums and rodents, major natural reservoirs of T. cruzi). Such a trend has been reported for R. pictipes, R. robustus, R. pallescens and R. colombiensis (Jaramillo et al. 2000; Palomeque et al. 2000; Vallejo et al. 2000). As bug colonies grow denser, the availability of food per individual declines. Starved bugs frequently start dispersive flights, and this behaviour seems to represent the main single source of Chagas disease transmission risk in the Amazon (Teixeira et al. 2001; Coura et al. 2002).

In spite of these observations, the attempts made to date to describe the links between palms, vectors, and epidemiological risk have been mainly qualitative. Barrett (1991) proposed that certain traits of some palm species (mainly a pattern of leaf abscission leaving old leaf bases attached to the trunk) may favour the establishment of Rhodnius colonies. Romaña et al. (1999) also suggested that the architectural characteristics of Attalea butyracea make it more suitable for R. pallescens than other palm species. In other cases, the presence of bird nests on palm crowns was the only factor apparently favouring infestation (Gurgel-Gonçalves et al. 2004).

Describing which traits of wild ecotopes favour triatomine infestation is a first step towards identifying ‘risk ecotopes’ (microhabitats where triatomine populations of species displaying synanthropic behaviour and potentially infected by T. cruzi occur near households). This is in turn required for epidemiological risk mapping, allowing for the design of rational surveillance-control strategies. Following this logic, we developed a novel fieldwork approach that explores relationships between selected ecological and botanical variables and the presence of Rhodnius colonies on palm trees. We tested this approach in Phytelephas aequatorialis, considered as the primary ecotope of R. ecuadoriensis– a major vector of Chagas disease in Ecuador and Peru (Aguilar et al. 1999; Abad-Franch et al. 2000, 2001; Cuba Cuba et al. 2002). The seed endosperm (vegetable ivory or ‘tagua’) and leaves of this economically important palm, endemic to W Ecuador, are used for handicraft manufacture and roof thatching; as a result, the palms are often typical of local anthropic landscapes (Henderson et al. 1995; Southgate 1997).

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study areas and bug trapping

The survey covered most of the climatic and altitudinal range of Ph. aequatorialis, encompassing three ecologically distinct areas in W Ecuador (Figure 1): (i) in the Andean foothills (wet premontane forest life zone), an area of approximately 5 km2 with small rural farms was surveyed [79° 00′W 00° 20′S, 900 m above sea level (m.a.s.l.), 56 palms]; (ii) in the central lowlands, we selected a heavily deforested area with extensive pasture fields (originally wet premontane forest, 79° 13′W 0° 19′S, 640 m.a.s.l., only three tagua palms found) and a remnant of old secondary forest and its fringes (moist tropical forest, 79° 32′W 0°12 ′S, 400 m.a.s.l., 15 palms); (iii) in the coastal region, two sites located within narrow valleys surrounded by low hills were surveyed (80° 20′W 1° 07′S and 80°15′W 1°02′S, 100 m.a.s.l. both, 18 palms on each site); localized rain and dense mist allow the growth of humid forests on the hills, generating a somewhat moist local climate in the valleys, where subsistence farming includes tagua harvesting. Phytelephas aequatorialis is rare in other areas of the central coast, dominated by arid life zones. The trapping method devised by Noireau et al. (1999) was used as described by Abad-Franch et al. (2000) and Noireau et al. (2002).

image

Figure 1. Ecology of sylvatic Rhodnius ecuadoriensis populations: fieldwork areas.

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Botanical and ecological variables

Several traits were recorded for each Ph. aequatorialis palm included in the survey: type of surrounding landscape (forest or anthropic); sex (Ph. aequatorialis is dioecious); height of stipe; and amount of epiphytic plants (EP) and of decomposing organic material (OM: dead leaves, husks, inflorescences-infrutescences and fibres from the palm itself, plus dead epiphytic-creeping plants). A semi-quantitative score up to ++++ was given to each palm for EP and OM (Figures 2 and 3). Individual mean values of EP and OM (the ‘organic score’, OS) were used for joint analysis of both variables.

image

Figure 2. Score of epiphytic plants growing on palm trees. Only living plants (both true epiphytes and creeping plants) were taken into account for this score. Intermediate values (1/2+, +1/2, ++1/2 and +++1/2) are not represented in the figure but were also used in the study.

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image

Figure 3. Score of decomposing organic matter (OM) on palm trees. Only dead organic material (dead leaves, fibres, dead epiphytes and other vegetable debris) was taken into account for this score. Note that minimum values were always >0. Intermediate values (+1/2, ++1/2 and +++1/2), not represented in the figure, were also used in the study.

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Statistical approaches

Parametric tests were used when the assumptions of normality and homoscedasticity were met, and non-parametric otherwise, to explore relationships between variables. Odds ratios (OR) and 95% confidence intervals (CIs) were calculated from logistic regression analysis. Other abbreviations used below are: χ2, chi-square; WT, Wilcoxon test; t, t-statistic from Student's t-test; LR, likelihood ratio test; d.f., degrees of freedom; P, significance probability; FET, Fisher's exact test and SD, standard deviation. Calculations were made using the JMP 4.0.4 software package (SAS Institute 2000).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Overall, 25 of 110 (22.7%) Ph. aequatorialis palm trees were found to be infested by R. ecuadoriensis. The number of bugs collected per infested palm was higher in the Andean foothills than in the coastal region (WT χ2 = 13.13, 1 d.f., P = 0.0003). Table 2 summarises general results and descriptive statistics.

Table 2. Rhodnius ecuadoriensis in Phytelephas aequatorialis palm trees in western Ecuador: entomological indices and characteristics of 110 palms surveyed
VariableFoothillsLowlandsCoastTotal
  1. M, mean; SD, standard deviation; Md, median; R, range.

  2. * Sex was not determined in 23 palms (mainly subadults).

Number of palms sampled (infested)56 (14)18 (1)36 (10)110 (25)
Infestation (%)255.5727.7822.73
Bugs captured143126170
Density (bugs/palms sampled)2.550.060.721.55
Crowding [bugs/infested palms (Md, R)]10.2 (9, 1–22)12.6 (2, 1–9)6.8 (6, 1–22)
Colonization [% infested with nymphs (n)]93 (13)100 (1)90 (9)92 (23)
Trap-nights used (M/palm sampled)88 (1.6)43 (2.4)91 (2.5)222 (2)
Trap-nights positive (%)29 (33)1 (2)15 (16.5)45 (20.3)
Palm stem height [M ± SD (m)]3.6 ± 1.64.4 ± 2.45.7 ± 1.64.5 ± 1.9
Palm sex ratio (♂:♀)*1:0.61:0.51:0.81:0.6
Organic matter [score M ± SD (Md)]1.8 ± 0.9 (1.5)1.8 ± 0.7 (1.75)1.7 ± 0.6 (1.5)1.8 ± 0.8 (1.5)
Epiphytic plants [score M ± SD (Md)]1.6 ± 1 (1.5)1 ± 0.5 (1)0.7 ± 0.5 (0.5)1.2 ± 0.9 (1)
Organic score [M ± SD (Md)]1.7 ± 0.9 (1.5)1.4 ± 5.4 (1.25)1.2 ± 0.3 (1.25)1.5 ± 0.7 (1.25)
Palms in anthropic/forest landscapes46/1010/836/092/18

Botanical variables and infestation

Landscape.  Palms located in anthropic landscapes (n = 92) were more frequently infested (>27%) than those within forest remnants (n = 18, FET P = 0.01).

Sex.  Male palms (n = 53) were more frequently infested (34%) than females (n = 34; 17.7%). This difference (not statistically significant) was larger on the coast (40%♂vs. 12.5%♀ infested; LR P = 0.059) than in the foothills (43%♂vs. 33%♀; LR P = 0.59); only two females were infested on the coast. Male palms had significantly larger amounts of OM than females (WT χ2 = 9.02, 1 d.f., P = 0.0027), but both sexes were similar in other respects. Sex-related OM differences were only significant in coastal palms (WT χ2 = 9.74, 1 d.f., P = 0.0018).

Stem height.  Stems of infested palms were taller (mean = 5.3 ± 1.7 m) than stems of non-infested palms (4.3 ± 1.9 m; t = 2.43, 108 d.f., P = 0.017). Considering infested palms only, stem height did not influence the apparent density of the colonies.

Decomposing organic matter.  The most significant differences between infested and non-infested palms were those recorded in OM scores (LR χ2 = 11, 1 d.f., P = 0.001; Figure 4).

image

Figure 4. Organic matter score (OM) and palm infestation: logistic regression plot showing the increase in the probability of palm infestation [p(i), y-axis] as a function of the organic matter score (OM, x-axis). LogLikelihood (reduced model − full model) = 5.5, χ2 = 11, 1 d.f., P = 0.0009. Broken arrows highlight values of OM for p(i) = 0.23 (observed) and p(i) = 0.5, and of p(i) for OM = 4 (maximum value).

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Epiphytes.  Epiphytes scores marginally correlated with the likelihood of infestation (LR χ2 = 3.9, 1 d.f., P = 0.049).

Organic score.  The OS was significantly higher among infested palms (LR χ2 = 8.6, 1 d.f., P = 0.003). Logistic regression yielded similar results for both female and male palms, but for α = 0.99 the association was only significant in males. Palms with OS > 1.25 (median value) were more frequently infested (FET P = 0.02; OR = 3.3, 95% CI = 1.3–8.6); this was not verified for female palms (FET P = 0.6), whereas the difference was marginally significant for males (FET P = 0.049) when analysed separately. The apparent density of bug colonies was also positively correlated with the OS of infested palms (quadratic fit, R2 = 0.68, P < 0.0001, n = 25; Figure 5).

image

Figure 5. Correlation between the ‘organic score’ in infested (n = 25) palm trees (x-axis) and the apparent density of bug colonies [as the number of bugs collected from each infested palm (y-axis)]: second-order polynomial fit.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Rhodnius ecuadoriensis is the second main vector of Chagas disease in Ecuador and in N Peru. It establishes dense colonies in both peridomestic and intra-domiciliary environments; the bugs are commonly infected by T. cruzi (5–10%, up to 56%) and eclectic feeders. In areas where R. ecuadoriensis is the predominant (or only) synanthropic vector species, the prevalence of anti-T. cruzi antibodies in humans is typically >5%, reaching >10% in some cases. Finally, mitochondrial DNA sequence analyses provided no indication of restricted gene flow between R. ecuadoriensis populations from palms and houses in Ecuador (cf. Abad-Franch et al. 2001; Cuba Cuba et al. 2002, 2003; Abad-Franch 2003; Abad-Franch & Aguilar 2003; Grijalva et al. 2005). A palm infested by R. ecuadoriensis is therefore to be considered as a ‘risk ecotope’ for people living nearby. Faced with this situation, field researchers need practical means for identifying which traits of individual palms may increase the likelihood of infestation. This report presents an attempt in that direction.

About 23% of the palms we studied were infested (27% considering only anthropic landscapes), with an average of approximately seven bugs/infested palm. Infestation did not follow a random pattern in our sample, with some palms being consistently more likely to be infested than others. We accordingly present a tentative operational description of ‘risk palm ecotope’ that illustrates the potential value of the approach described here.

Infested Ph. aequatorialis were generally adult trees, often with stems >3 m (26.4% infested, vs. only one palm <3 m tall (4.6%); FET P = 0.02). They were located in anthropic landscapes (generally near human dwellings) rather than in forests. Many were classified as ‘dirty’ [OM scores > 1.5 (median OM value) increased three times the odds of a palm being infested (OR = 2.9, 95% CI = 1.2–7.8)]. This trait was more frequent among male palms, and the single most important factor favouring infestation. Infested palms did also present relatively large amounts of epiphytic plants growing around their stipes and on their crowns. Phytelephas aequatorialis palms with stems above 3 m, sited in an anthropic landscape and with an OM score > median value had in our sample a probability slightly above 0.57 (12 of 21) of harbouring R. ecuadoriensis. Within this group, 81% were males, 77% of which were infested. R. ecuadoriensis seems only able to form relatively small colonies on these palms, but the risk posed by the ability of the bugs to invade and colonize human habitats cannot be neglected.

Triatomines are nest-dwelling bugs; they thrive only under adequate microenvironmental conditions (mainly a buffered microclimate and a regular food supply; cf. Schofield 1994). Considering the diversity and architectural complexity of palm microhabitats, a few authors have proposed that specific, and even individual, variation among palms might have a bearing on the likelihood of infestation (Pizarro & Romaña 1998; Luz et al. 1999; Romaña et al. 1999; Jaramillo et al. 2000). Our results largely support the notion that differential suitability for bug colonization is linked to microenvironment-related individual palm traits, while suggesting that other factors (involved in the ecological dynamics of anthropic landscapes) may also be important. Surveys exploring potentially relevant variables (ecological macroregions, soil characteristics, land use patterns, phytogeography and anthropogenic palm dispersal, presence of putative vertebrate hosts on the palms, etc.) are ongoing.

The findings of our survey also suggest that human activities may alter the dynamics of sylvatic populations of R. ecuadoriensis inhabiting Ph. aequatorialis. Thus, infestation is more common in anthropic landscapes (where palms are preserved near houses), while pruning of female palms in areas of tagua harvesting (such as the coastal region) results in lower infestation rates.

Our observations can contribute to current efforts to define rational surveillance-control interventions in areas where sylvatic triatomine populations are potentially involved in T. cruzi transmission to people. In this sense, a strategy we might call ‘integrated habitat management’ could help reduce transmission mediated by palm tree-living R. ecuadoriensis. It would combine: (i) tracing areas where Ph. aequatorialis grow near houses (following tagua trade routes and/or using RS-GIS) and describing local transmission profiles and risk factors; (ii) spraying infested dwellings and promoting better poultry management (cf. Abad-Franch et al. 2002); (iii) in areas of tagua harvesting, removing dead fronds and other organic debris could reduce both palm infestation rates and the density of bug colonies. In some cases, high-risk palm trees could be treated with insecticides or even eliminated from peridomiciles. Health risks linked to tagua harvesting must be advertised to the locals and to organizations that foster this activity (e.g. Southgate 1997); (iv) community-based entomological surveillance will be crucial to detect and eliminate reinfesting bugs in areas where control of R. ecuadoriensis is undertaken and Ph. aequatorialis palms are present near houses. The implementation of longitudinal, community-based disease control-surveillance strategies is a challenging matter. Results from Chagas disease vector control programmes in several countries show, however, that they are cost-effective, enhance self-esteem and result in community empowerment regarding health and quality of life issues. This may in addition be the best-fitted strategy in the current context of health services decentralization in most Latin American countries (Bryan et al. 1994; Dias 1998, 2000).

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Funding by the WHO TDR programme (ID 970195) and the ECLAT Network is gratefully acknowledged. A. Paucar, C. Carpio, K. Suárez, A. Abad-Franch, and the workers of the Ecuadorian Malaria Control Service gave most valuable assistance during fieldwork. Comments by one anonymous referee significantly helped to improve the original manuscript.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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