The Effects of Eisenia fetida Lumbricidae and Vermicomposting on Earthworm Populations in Monteverde, Costa Rica Sibylle Freiermuth Department of Biology, Denison University ABSTRACT Eisenia fetida Lumbricidae is an African earthworm species used in vermicomposting in the larger Monteverde region of Costa Rica. Despite its widespread use and growing popularity, little is known about the impact that introducing E. fetida has on local earthworm species. Exotic earthworms have the potential to drasti cally change the soil composition and community structure causing cascading effects throughout the ecosystem. However, previous studies have found signs of possible niche partitioning and that species richness and abundance actually increased in the presen ce of E. fetida . Taking samples for six farms using vermicomposting and six without, I found that vermicomposting actually increased the species richness of earthworm communities when considering all samples collectively H = 1.09, 0.78, t = 2.30, df = 267 , P < 0.05 , when only considering non coffee farms H = 0.78, 0.39, t = 2.13, df = 60, P < 0.05, and when comparing non coffee farms to coffee farms H = 1.05, 0.70, t = 2.28, df = 114, P < 0.05. However, when looking at other subsets only including farms having applied vermicompost within the last year, excluding farms using greenhouses, and only considering coffee plantations there was no significant difference in earthworm communities. Based on this study, it seems that although E. fetida is enteri ng farm soils, there is no negative impact on preexisting earthworm populations. RESUMEN Eisenia fetida Lumbricidae es una especie de lombriz africana que es usada para compostaje vermicular en la regiÃ³n de Monteverde, Costa Rica. A pesar del uso ext endido y de la popularidad del abono, no mucho es conocido sobre el impacto que E. fetida tiene en los lombrices locales. Lombrices exÃ³ticas puedan cambiar la composiciÃ³n del suelo y la estructura de la comunidad drÃ¡sticamente, causando efectos sobre todo el ecosistema. Sin embargo, estudios previos han indicado la posibilidad de que compartan nicho y que la riqueza de especies y la abundancia se aumenta cuando E. fetida estÃ¡ presente. Muestreando seis fincas que usan el abono de los lombrices y seis sin E . fetida , descubrÃ que el compostaje vermicular aumenta la riqueza de especies de la comunidad de los lombrices teniendo en cuenta todos las muestras H = 1.09, 0.78, t = 2.30, df = 267, P < 0.05 , cuando solo se toman en cuenta fincas sin cafÃ© H = 0.7 8, 0.39, t = 2.13, df = 60, P < 0.05, y comparando las fincas sin cafÃ© con las de cafÃ© H = 1.05, 0.70, t = 2.28, df = 114, P < 0.05 Sin embargo, al analizar diferentes subconjuntos solo teniendo en cuenta fincas que han usado el abono durante el aÃ±o pa sado, excluyendo la finca que usa invernaderos, y solo teniendo en cuenta las fincas de cafÃ© no hay una diferencia significativa en las comunidades de lombrices. Basado en esta investigaciÃ³n , parece que aunque E. fetida estÃ¡ entrando en el suelo de las fin cas, no hay un impacto negativo en las poblaciones de lombrices preexistentes. .
INTRODUCTION In an attempt to increase the sustainability of coffee production, the Fair Trade Cooperative of Santa Elena, Costa Rica is using the earthworm Eisenia fetid a to vermicompost the coffee pulp waste material. Independent farmers are also beginning to use E. fetida as a source of organic fertilizer as the rising price of chemical fertilizer makes vermicomposting more economically favorable and as it offers a more organic source of fertilizer N. Santamaria Brenes and M. Perez Cespedes, pers. comm., 2008. The compost that is applied on the farms contains both eggs as well as live worms, thereby introducing E. fetida to the farm soil . At this point, still not enoug h is known about the impact that the introduction of E. fetida has on native earthworm populations to determine whether vermicomposting is ecologically viable in the long term. It is imperative to understand the impact of introducing E. fetida to local far ms as it could potentially not only affect the earthworm community but also influence the productivity of a major agricultural crop and source of income for the Monteverde region. Although earthworms are generally beneficial for the soil by increasing the availability of nutrients for other organisms and because their relatively stable tunnels aid in air and water flow Kladiviko 1993, if introduced into a new environment earthworms can potentially upset the preexisting natural equilibrium. Invasion of non native earthworms has already significantly altered soil composition and flora and fauna communities in Northern America Bohlen et al. 2004. In his Â€Ecological Risk Assessment of Non indigenous Earthworm SpeciesÂ, Proulx 2003 highlights that different rates of leaf litter cycling of particular concern with E. fetida can directly impact the plant communities dependent on layers of organic matter and that this change can then impact other organisms higher in the food chain. Exotic earthworms may also c ompete with native earthworms for resources, although Hendrix et al. 2006 found that competitive exclusion of native earthworms is not easily demonstrated and that co existence is common. However, a study of the relationship between the exotic Pontoscole x corethrurus and native species in the Caribbean coast of Costa Rica found P. corethrurus to be largely dominant in every site and almost all habitat types as well as a significant reduction in the rest of the earthworm fauna Lapied and Lavelle 2003. No definitive analysis of the effect of E. fetida on earthworm populations currently exists, although several previous studies provide useful insights. Askham 2007 found significant niche partitioning in preference for organic soil content between E. fet ida and native species, indicating the possibility of limited competition between the two. However, he found no difference in preferences for humidity/moisture and soil texture. Lapachin 1996 found different bread consumption rates between E. fetida and a native species which could indicate different preferences or niches, but could also mean that E. fetida may out compete native species. Neuhauser et al. 1980 found that E. fetida growth is directly related to population density; therefore, the increase in population density may result in an overall decline in growth. All these factors combined indicate that when introduced as an exotic species , E. fetida may dominate over native species, just as the exotic species dominated in both secondary growth fores t and plantations in a study conducted in Puerto Rico Gonzalez et al. 1996. However, the most relevant study conducted to date on earthworm populations and E. fetida in the
Monteverde region found that abundance and species richness of all earthworms com bined positively correlated to E. fetida abundance Gaechter 2004. Based on the findings of these previous studies, I expected the presence of E. fetida to have an impact on the overall earthworm community, possibly altering species richness or diversity . I anticipated that since invasive species have been known to alter soil conditions and dominate over native species that native earthworm richness and abundance would decline in the presence of E. fetida , despite the preliminary findings of Gaechter 20 04. METHODS Study Site I conducted the study between July 15 and 31, 2008 in the Monteverde region of Costa Rica. I compared earthworm species richness and abundance in two habitats: farms using vermicomposting from E. fetida and those without vermicomposting . I sampled six farms in each habitat, all located between La Cruz and San Luis, ranging in elevation from 1000 m to 1500 m. Half of the non vermicomposting farms cultivated coffee while the other samples came from other crops. Four of the vermicompostin g farms cultivated coffee while the other two were vegetable gardens. Three of the farms had their own vermicomposting facility while the other three used compost provided by the Santa Elena Coffee Cooperative. All farms differed in length and frequency of vermicomposting application, and one differed from the others by using greenhouses. Data Collection At every farm I sampled four different 30 x 30 cm wide and 20 cm deep soil plots. These dimensions should be deep enough to include both litter dwellers and shallow soil dwellers that live primarily in the top layer of soil but should exclude deep burrowers that can dig up to two meters deep Kladivko 1993. I searched through the soil by hand, counting and identifying according to morphospecies on site. For each sample I recorded the number of individuals of each morphospecies found. I determined morphospecies predominantly based on color, behavior, size, and distinctive visible organs. I took digital photographs to aid in comparison of morphospecies between sites and for future reference Appendix I. The collective number of individuals and morphospecies per each farm type were analyzed using the Shannon Weiner Diversity Index and a t test. I also repeated the analysis for several different subsets, separat ing the coffee from the non coffee farms, excluding the samples from greenhouses, excluding farms not having used vermicomposting within the last year, and comparing coffee plantations to other farms regardless of vermicomposting use. RESULTS I collected a to tal of 296 worms that I classified into eight different morphospecies Table 1. I found a higher species richness in farms using vermicomposting, while evenness was similar between the two farm types. I also found a significant difference in the
Shannon W einer Diversity Index and Marglaf s Species Index between farms using vermicomposting from E. fetida and those without Figure 1. Table 1. Total number of each morphospecies collected on farms using vermicomposting and those without, and the total number o f individual worms collected at each farm type. Morphospecies Using Vermicomposting Non vermicomposting Eisenia fetida 9 0 Pink head 136 85 Large, active dark 8 4 Short, fat, grey 10 1 Medium, grey 11 8 All light pink 3 0 Small jumping 4 11 Medium reddish 6 0 total 187 109 Figure 1. Species richness S X 10 1 , Marglaf s Species S marg , Shannon Weiner diversity H , and evenness E indices for farms using E. fetida vermicomposting and those without in the Monteve rde region of Costa Rica. N = 187 vermicomposting and 109 non vermicomposting, t = 2.30, df = 267, P < 0.05. However, when the data were analyzed in a subset excluding the one farm using greenhouse tents the difference was no longer significant. The number of earthworms per sample for farms using vermicomposting decreased from 187 to 174, while species richness 8, 5, Marglaf s species index 1.36, 0.85, and evenness 0.48, 0.49 did not change significantly. The Shannon Weiner diversity index 1 .09, 0.78 was no longer significantly different t = 1.58, df = 265, P < 0.05. A second subset only including the farms having used vermicomposting within the last year also showed no significant difference. Species richness decreased from eight to six, N decreased from 187 to 85, and Marglaf s index decreased from 1.34 to 1.13 in the farms using vermicomposting while evenness did not change significantly from 0.53 to 0.56. Shannon Weiner diversity index 1.00, 0.78 was no longer significantly different t = 1.43, df = 177, P < 0.05. 0.80 1.34 1.09 0.53 0.50 0.85 0.78 0.49 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 S Smarg H' E Using Vermicomposting Non-vermicomposting
When only comparing the earthworm populations in non coffee samples, sample size 23 and 39 and species richness decreased in both farm types, while the differences in the other factors increased Figure 2. However, whe n only comparing earthworm populations in coffee samples, the indices were no longer statistically different t = 0.65, df = 238, P < 0.05. The number of earthworms per sample was 164 and 70 while species richness was 8 and 5 for vermicomposting and non v ermicomposting farms respectively. Figure 2. Species richness S X10 1 , Marglaf s Species S marg , Shannon Weiner diversity H , and evenness E indices for non coffee farms using E. fetida vermicomposting and those witho ut in the Monteverde region of Costa Rica t = 2.13, df = 60, P < 0.05. Another subset of data comparing earthworm populations between farms cultivating coffee and those with other crops not taking vermicomposting into account also found a significan t difference between the two. The number of earthworms per sample was 234 for coffee plantations and 62 for non coffee farms Figure 3. Smarg = 0.96919548 H' = 0.70 E = 0.43457342 0.8 1.28 1.05 0.51 0.50 0.97 0.70 0.43 0 0.2 0.4 0.6 0.8 1 1.2 1.4 S Smarg H' E coffee non-coffee Figure 3. Species richness S X 10 1 , Marglaf s Species S marg , Shannon Weiner diversit y H , and evenness E indices for coffee and non coffee farms regardless E. fetida vermicompost use in the Monteverde region of Costa Rica t = 2.28, df = 114, P < 0.05. 0.30 0.64 0.78 0.71 0.30 0.55 0.39 0.35 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 S Smarg H' E Vermicomposting in noncoffee Non-vermicomposting in non-coffee
DISCUSSION The data indicate that at least under certain circumstances E. fetida does affect earthworm population richness, although in all cases where there was a significant difference, richness was higher in the presence of vermicomposting . This indicates that the findings of Gaechter 2004 were right in showing that the presence of E. fetida actually positively correlates with species richness, and that E. fetida is not negatively impacting native earthworm populations as originally predicted. However, the difference in H were rendered insignificant by excluding the farm using gree nhouses and by only including farms having used vermicomposting recently. There was also no significant difference found when only comparing the farms cultivating coffee. This lack of significance when only considering certain subsets of data indicates that t he effects of adding vermicomp osting and E. fetida are less significant than the influence of other variables. The subset only considering farms having used vermicomposting within the last year is particularly interesting, because the results are counterintuitiv e; one would expect the effects of E. fetida to increase rather than decrease with more recent and increased application frequency. However, this subset also excludes the farm using greenhouses, showing that potentially the samples from a single farm can s ignificantly influence the entire data set. Despite the significant results when considering all samples together, the study still does not conclusively reveal the effects of using E. fetida vermicomposted fertilizer. It is possible that the richer soil g enerally associated with composting and/ or the lack of potentially toxic chemical fertilizers used on non composting farms, rather than the presence of E. fetida actually affect the earthworm community. The finding of a significant difference in earthworm populations when only comparing farms cultivating coffee and those from other crops disregarding vermicomposting use also suggests that the surrounding vegetation and cultivation practices may be more important factors than E. fetida. Although difference in species richness is not consistent across all parameters, there is a consistent difference in number of worms found per farm. One hundred and eighty seven of the total 296 worms collected were found in farms using vermicomposting, a difference that cann ot be attributed to the inclusion of the nine E. fetida found. Therefore, the data seem to indicate that either the presence of E. fetida or vermicomposting not only affects species richness but also abundance of earthworms. Based on these data, it seems tha t the use of vermicomposting and particularly the introduction of E. fetida is not having a negative impact on local earthworm populations. This is of great significance as more farmers are becoming interested in using E. fetida and as vermicomposting seem s to offer a more natural and organic alternative to potentially harmful chemical fertilizers. The farmers already using vermicomposting expressed a strong preference for this method, praising the long term sustainability of the method C. Abarca Arias, pe rs. comm., although vermicomposting has not been used and studied long enough to substantiate their claim. It is still not clear what some of the long term effects of introducing E. fetida may be. It is possible that minor alterations in environmental con ditions, such as are occurring fairly rapidly in the montane region of Monteverde Pounds et al. 1999, may change earthworm population dynamics in such a way that E. fetida could have a different effect on local earthworm species. In order to test potenti al future impact, I suggest
experimenting on the different environmental preferences of different species and elaborating on the preliminary findings of Askham 2007. Although it seems that E. fetida is not having a negative impact on earthworm species r ichness in general, little is known about its effect on individual earthworm species. To determine this, I suggest studying individual species in isolation with E. fetida . Not enough is known about the impact of E. fetida on the larger community as well. If E. fetida really increases earthworm species richness and abundance, this could result in increased leaf litter decomposition or alterations in soil composition, thereby influencing the plant community just as Proulx 2003 warns in his Ecological Risk Assessment of Non indigenous Earthworms. Since there are still so many unknown variables, further study is needed to determine the full impact of vermicomposting and the introduction of E. fetida . ACKNOWLEDGMENTS I would like to thank Karen Masters for b eing my advisor and for being part of the process from initial idea to final analysis. I would also like to thank Carlos Abarca Arias, Finca El Jardin, Gilber Lobo, La Escuela Creativa, Mario Perez Cespedes, Meg and Richard LaVal, Milton Salazar, Norman Sa ntamaria Brenes, Odilie Mora Burgos, Oldemar Salazar, and Xinia Araya LeitÃ³n , for letting me use their farms as study sites and for being willing to share their insights with me. Thank you also to Noe Vargas LeitÃ³n and Guillermo Vargas LeitÃ³n for helping m e find all my contacts. Finally, I d like to thank my host family Perez Picado who lent me their tools and provided me a home base for my study. A special thanks also goes to Crystel who enthusiastically helped me dig for worms. LITERATURE CITED As kham, C. 2007. Niche partitioning between Eisenia foetida Lumbricidae and native earthworms in Monteverde, Costa Rica. 199 207.Tropical Ecology and Conservation. CIEE, Fall. Bohlen, P. J., S. Scheu, C. M. Hale, M. A. McLean, S. Mingge, P. M. Groffman, a nd D. Parkinson. 2004. Non Native Invasive Earthworms as Agents of Change in Northern Temperate Forests. Frontiers in Ecology and Environment. 28: 427 435. Gaechter, L. 2004. Colonizing limitations of the composting earthworm Eisenia foetida . 161 168. Tr opical Ecology and Conservation. CIEE, Spring. Gonzalez, G., X. Zou, and S. Borges. 1996. Earthworm abundance and species composition in abandoned tropical croplands: comparison of tree plantations and secondary forests. Pedobiologia. 40: 385 391. Hendr ix, P., G. H. Baker, M.A. Callaham, G.A. Damoff, C. Fragoso, G. Gonzalez, S.W. James, S. L Lachnicht, T. Winsome, and X. Zou. 2006. Invasion of exotic earthworms into ecosystems inhabited by native earthworms. Biological Invasions. 8: 1287 1300. Kladivko, E. J. 1993. Earthworms and crop management. Agronomy Guide. Cooperative Extension Work in Agriculture Lapachin, J. 1996. Contrasting vermicomposting rates between two worms: Eisenia foetida and a Native Worm. Tropical Ecology and Conservation. 93 104. CIEE , Summer.
Lapied, E. and P. Lavelle. 2003. The peregrine earthworm Pontoscolex corethrurus in the East coast of Costa Rica. The 7 th international symposium on earthworm ecology. Neuhauser, E. F., R. Hartenstein, and D. L. Kaplan. 1980. Growth of earthworm Eisenia foetida in relation to population density and food rationing. Oikos. 35: 93 98. Pounds, J. A., M. P. L. Fogden, and J. H. Campbell.1999. Biological response to climate change on a tropical mountain. Nature. 398: 611 614. Proulx, N. 2003. Ecological Risk Assessment of Non indigenous Earthworm Species. US Fish and Wildlife Service. UC Sustainable Agriculture Research and Education Program. 2008. Eisenia foetida Savigny Lumbricidae. < http://www.sarep.ucdavis.edu/worms/>. Accessed July 2, 2008.
APPENDIX I Morphospecies Three of the morphospecies I identified. Morphospecies pink head : distinctive pink head, grey body, lighter grey posterior varied some in darkness. Based on descriptions this may be Pontoscol ex corethrurus MÃ¼ller. Morphospecies: short, fat, grey : all grey body, distinctive segmentation, lobed end. cut in half by trowel Morphospecies: Large, active, dark : long dark bodies, thrash/jump about when disturbed in whiplike bo dy motion; have distinctive segment at anterior end.
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Los efectos de Eisenia fetida (Lumbricidae) y vermicompostaje sobre las poblaciones de lombrices de tierra en Monteverde, Costa Rica.
The effects of Eisenia fetida (Lumbricidae) and vermicomposting on earthworm populations in Monteverde, Costa Rica
Eisenia fetida (Lumbricidae) is an African earthworm species used in vermicomposting in the larger Monteverde region of Costa Rica. Despite its widespread use and growing popularity, little is known about the impact that introducing E. fetida has on local earthworm species. Exotic earthworms have the potential to drastically change the soil composition and community structure causing cascading effects throughout the ecosystem. However, previous studies have found signs of possible niche partitioning and that species richness and abundance actually increased in the presence of E. fetida. Taking samples for six farms using vermicomposting and six without, I found that vermicomposting actually increased the species richness of earthworm communities when considering all samples collectively (H= 1.09, 0.78, t = 2.30, df = 267, P < 0.05 ), when only considering non-coffee farms (H = 0.78, 0.39, t = 2.13, df = 60, P < 0.05), and when comparing non-coffee farms to coffee-farms (H = 1.05, 0.70, t = 2.28, df = 114, P < 0.05). However, when looking at other subsets only including farms having applied vermicompost within the last year, excluding farms using greenhouses, and only considering coffee plantations there was no significant difference in earthworm communities. Based on this study, it seems that although E. fetida is entering farm soils, there is no negative impact on preexisting earthworm populations.
Eisenia fetida (Lumbricidae) es una especie de lombriz africana que es usada para compostaje vermicular en la regin de Monteverde, Costa Rica. A pesar de su uso comn y de la popularidad del abono, poco se sabe sobre el impacto que E. fetida tiene en las lombrices locales. Las lombrices exticas pueden cambiar la composicin del suelo y la estructura de la comunidad drsticamente, causando efectos sobre todo el ecosistema. Sin embargo, estudios previos han indicado la posibilidad de que compartan nichos y que la riqueza de especies y la abundancia aumenta cuando E. fetida esta presente.
Text in English.
Eisenia fetida--Costa Rica--Puntarenas--Monteverde Zone
Earthworms--Ecology--Costa Rica--Puntarenas--Monteverde Zone
Eisenia fetida-- Costa Rica
Lombrices de tierra--Ecologa--Costa Rica--Puntarenas--Zona de Monteverde
Tropical Ecology 2008
Ecologa Tropical 2008
t Monteverde Institute : Tropical Ecology