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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 widesp read use and growing popularity, little is known ab out the impact that introducing E. fetida has on local earthworm species. Exotic earthworms have the potential to drastically change the soil composition and comm unity structure causing cascading effects throughou t the ecosystem. However, previous studies have found signs of possible niche partitioning and that spec ies richness and abundance actually increased in the pr esence of E. fetida Taking samples for six farms using vermicomposting and six without, I found that vermi composting 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 whe n comparing non-coffee farms to coffee-farms (H = 1. 05, 0.70, t = 2.28, df = 114, P < 0.05). However, w hen looking at other subsets only including farms havin g applied vermicompost within the last year, exclud ing farms using greenhouses, and only considering coffe e plantations there was no significant difference i n earthworm communities. Based on this study, it seem s that although E. fetida is entering farm soils, there is no negative impact on preexisting earthworm populat ions. RESUMEN Eisenia fetida (Lumbricidae) es una especie de lombriz africana qu e es usada para compostaje vermicular en la region de Monteverde, Costa Rica. A pesar del uso extendido y de la popularidad del abono, no mucho es conocido sobre el impacto que E. fetida tiene en los lombrizes locales. Lombrices exticas puedan cambiar la composicin del suelo y la estruc tura de la comunidad drsticamente, causando efecto s sobre todo el ecosistema. Sin embargo, estudios pre vios han indicado la posibilidad de que compartan nicho y que la riqueza de especies y la abundancia se aumenta cuando E. fetida esta presente. Muestreando seis fincas que usan el abono de los lombrices y se is sin E. fetida descubr que el compostaje vermincular aumenta la riqueza de especies de la comunidad de l os lombrices teniendo en cuenta todos las muestras (H= 1.09, 0.78, t = 2.30, df = 267, P < 0.05 ), cu ando solo se toman en cuenta fincas sin caf (H = 0.78, 0.39, t = 2.13, df = 60, P < 0.05), y comparando la s fincas sin caf con las de caf (H = 1.05, 0.70, t = 2.28, df = 114, P < 0.05) Sin embargo, al analizar difere ntes subconjuntos solo teniendo en cuenta fincas qu e han usado el abono durante el ao pasado, excluyendo la finca que usa invernaderos, y solo teniendo en cue nta las fincas de caf no hay una diferencia significat iva en las comunidades de lombrices. Basado en esta investigacion, parece que aunque E. fetida esta entrando en el suelo de las fincas, no hay un impacto negativo en las poblaciones de lombrices preexisten tes. INTRODUCTION
In an attempt to increase the sustainability of cof fee production, the Fair Trade Cooperative of Santa Elena, Costa Rica is using the earthworm Eisenia fetida to vermicompost the coffee pulp waste material. Indepe ndent farmers are also beginning to use E. fetida as a source of organic fertilizer as the rising pr ice of chemical fertilizer makes vermicomposting more economically favorable a nd as it offers a more organic source of fertilizer (N. Santamaria Brenes and M. P erez Cespedes, pers. comm., 2008). The compost that is applied on the farms contains b oth eggs as well as live worms, thereby introducing E. fetida to the farm soil At this point, still not enough is known about the impact that the introduction of E. fetida has on native earthworm populations to determine whether vermicomposting is ecologically v iable in the long-term. It is imperative to understand the impact of introd ucing E. fetida to local farms as it could potentially not only affect the earthworm community but also influence the productivity of a major agricultural crop and sourc e of income for the Monteverde region. Although earthworms are generally beneficial for th e soil by increasing the availability of nutrients for other organisms and because their rel atively stable tunnels aid in air and water flow (Kladiviko 1993), if introduced into a n ew environment earthworms can potentially upset the preexisting natural equilibri um. Invasion of non-native earthworms has already signi ficantly altered soil composition and flora and fauna communities in Nort hern America (Bohlen et al. 2004). In his Ecological Risk Assessment of Non-indigenou s Earthworm Species, Proulx (2003) highlights that different rates of leaf-litt er cycling (of particular concern with E. fetida ) can directly impact the plant communities depende nt on layers of organic matter and that this change can then impact other organism s higher in the food chain. Exotic earthworms may also compete with native earthworms for resources, although Hendrix et al. (2006) found that competitive exclusion of nati ve earthworms is not easily demonstrated and that co-existence is common. Howev er, a study of the relationship between the exotic Pontoscolex corethrurus and native species in the Caribbean coast of Costa Rica found P. corethrurus to be largely dominant in every site and almost al l 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 pref erence for organic soil content between E. fetida 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 cons umption rates between E. fetida and a native species which could indicate different prefe rences 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 a exotic species, E. fetida may dominate over native species, just as the exotic species dominated in bo th secondary growth forest and plantations in a study conducted in Puerto Rico (Go nzalez 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 combined 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 communit y, possibly altering species richness or diversity. I anticipated that since inv asive species have been known to alter soil conditions and dominate over native species, t hat native earthworm richness and abundance would decline in the presence of E. fetida despite the preliminary findings of Gaechter (2004). 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 abu ndance in two habitats: farms using vermicompost from E. fetida and those without vermicompost. I sampled six farm s in each habitat, all located between La Cruz and San L uis, ranging in elevation from 1000 m to 1500 m. Half of the non-vermicomposting farms cu ltivated coffee while the other samples came from other crops. Four of the vermicom posting farms cultivated coffee while the other two were vegetable gardens. Three o f 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 an d frequency of vermicompost application, and one differed from the others by us ing greenhouses. Data Collection At every farm I sampled four different 30 x 30 cm w ide and 20 cm deep soil plots. These dimensions should be deep enough to include both li tter-dwellers and shallow-soil dwellers that live primarily in the top layer of so il but should exclude deep-burrowers that can dig up to two meters deep (Kladivko 1993). I se arched 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 fou nd. I determined morphospecies predominantly based on color, behavior, size, and d istinctive visible organs. I took digital photographs to aid in comparison of morphospecies b etween sites and for future reference (Appendix I). The collective number of individuals and morphospec ies per each farm type were analyzed using the Shannon-Weiner Diversity Index a nd a t-test. I also repeated the analysis for several different subsets, separating the coffee from the non-coffee farms, excluding the samples from greenhouses, excluding f arms not having used vermicompost within the last year, and comparing coffee plantati ons to other farms regardless of vermicompost use. RESULTS I collected a total of 296 worms that I classified into eight different morphospecies (Table 1). I found a higher species richness in farms usin g vermicomposting, while evenness was similar between the two farm types. I also foun d a significant difference in the Shannon-Weiner Diversity Index and Marglafs Specie s Index between farms using vermicompost from E. fetida and those without (Figure 1).
Table 1. Total number of each morphospecies collect ed on farms using vermicomposting and those without, and the total number of individu al 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 n n r Figure 1. Species richness (S) (X 10-1), Marglafs Species (Smarg), Shannon-Weiner diversity (H), and evenness (E) indices for farms using E. fetida vermicomposting and those without in the Monteverde region of Costa Ric a. N = 187 (vermicomposting) and 109 (non-vermicomposting), t = 2.30, df = 267, P < 0.05. However, when the data were analyzed in a subset ex cluding the one farm using greenhouse tents the difference was no longer signi ficant. The number of earthworms per sample for farms using vermicomposting decreased fr om 187 to 174, while species richness (8, 5), Marglafs species index (1.36, 0.8 5), 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 us ed vermicompost within the last year also showed no significant difference. Sp ecies richness decreased from eight to six, N decreased from 187 to 85, and Marglafs inde x 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).
When only comparing the earthworm populations in n on-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, when 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 s ample was 164 and 70 while species richness was 8 and 5 for vermicomposting and non-ve rmicomposting farms respectively. n r rr "" !r "" Figure 2. Species richness (S) (X10-1), Marglafs Species (Smarg), Shannon-Weiner diversity (H), and evenness (E) indices for non-c offee farms using E. fetida vermicomposting and those without in the Monteverde region of Costa Rica (t = 2.13, df = 60, P < 0.05). Another subset of data comparing earthworm populat ions between farms cultivating coffee and those with other crops (not taking vermicomposting into account) also found a significant difference between the two The number of earthworms per sample was 234 for coffee plantations and 62 for no n-coffee farms (Figure 3). n n n n n r "" "" Figure 3. Species richness (S) (X 10-1), Marglafs Species (Smarg), Shannon-Weiner diversity (H), and evenness (E) indices for coffe e and non-coffee farms regardless E. fetida vermicompost use in the Monteverde region of Costa Rica (t = 2.28, df = 114, P < 0.05).
DISCUSSION The data indicate that at least under certain circu mstances E. fetida does affect earthworm population richness, although in all cases where th ere was a significant difference, richness was higher in the presence of vermicompost This indicates that the findings of Gaechter (2004) were right in showing that the pres ence 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 insigni ficant by excluding the farm using greenhouses and by only including farms havin g used vermicompost 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 the effects of adding vermicompost a nd E. fetida are less significant than the influence of other variables. The subset only c onsidering farms having used vermicompost within the last year is particularly i nteresting, because the results are counterintuitive; one would expect the effects of E. fetida to increase rather than decrease with more recent and increased application frequenc y. However, this subset also excludes the farm using greenhouses, showing that potentiall y the samples from a single farm can significantly influence the entire data set. Despite the significant results when considering al l samples together, the study still does not conclusively reveal the effects of u sing E. fetida vermicomposted fertilizer. It is possible that the richer soil generally assoc iated with composting and/ or the lack of potentially toxic chemical fertilizers used on noncomposting farms, rather than the presence of E. fetida actually affect the earthworm community. The findi ng of a significant difference in earthworm populations whe n only comparing farms cultivating coffee and those from other crops (disregarding ver micompost use) also suggests that the surrounding vegetation and cultivation practices ma y be more important factors than E. fetida. Although difference in species richness is not cons istent 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 cannot be attrib uted to the inclusion of the nine E. fetida found. Therefore, the data seem to indicate that e ither the presence of E. fetida or vermicompost not only affects species richness but also abundance of earthworms. Based on these data, it seems that the use of vermi composting 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 b ecoming interested in using E. fetida and as vermicomposting seems to offer a more natura l and organic alternative to potentially harmful chemical fertilizers. The farme rs already using vermicomposting expressed a strong preference for this method, prai sing the long-term sustainability of the method (C. Abarca Arias, pers. comm.), although ver micomposting has not been used and studied long enough to substantiate their claim It is still not clear what some of the long-term ef fects of introducing E. fetida may be. It is possible that minor alterations in enviro nmental conditions, 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 potent ial future impact, I suggest
experimenting on the different environmental prefer ences 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 richness in general, little is known about its effect on individual earthworm species. To determine this, I suggest studying indi vidual 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 ab undance, this could result in increased leaf-litter decomposition or al terations in soil composition, thereby influencing the plant community just as Proulx (200 3) warns in his Ecological Risk Assessment of Non-indigenous Earthworms. Since the re 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 being my ad visor and for being part of the process from initia l idea to final analysis. I would also like to thank Carlo s Abarca Arias, Finca El Jardin, Gilber Lobo, La Es cuela Creativa, Mario Perez Cespedes, Meg and Richard LaV al, Milton Salazar, Norman Santamaria Brenes, Odilie Mora Burgos, Oldemar Salazar, and Xinia Aray a Leiton, for letting me use their farms as study s ites and for being willing to share their insights with me. Thank you also to Noe Vargas Leiton and Guiller mo Vargas Leiton for helping me find all my contacts. Finally, Id like to thank my host family (Perez Pi cado) who lent me their tools and provided me a home base for my study. A special thanks also goes to Cryst el who enthusiastically helped me dig for worms. LITERATURE CITED Askham, C. 2007. Niche partitioning between Eisenia foetida (Lumbricidae) and native earthworms in Monteverde, Costa Rica. 199-207.Tropi cal Ecology and Conservation. CIEE, Fall. Bohlen, P. J., S. Scheu, C. M. Hale, M. A. McLean, S. Mingge, P. M. Groffman, and D. Parkinson. 2004. Non-Native Invasive Earthworms as Agents of Change in Northern Temperate Forests. Frontiers in Ecology an d Environment. 2(8): 427435. Gaechter, L. 2004. Colonizing limitations of the co mposting earthworm Eisenia foetida 161-168. Tropical Ecology and Conservation. CIEE, S pring. Gonzalez, G., X. Zou, and S. Borges. 1996. Earthwor m abundance and species composition in abandoned tropical croplands: compar ison of tree plantations and secondary forests. Pedobiologia. 40: 385-391. Hendrix, P., G. H. Baker, M.A. Callaham, G.A. Damof f, 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 eart hworms. Biological Invasions. 8: 1287-1300. Kladivko, E. J. 1993. Earthworms and crop managemen t. Agronomy Guide. Cooperative Extension Work in Agriculture Lapachin, J. 1996. Contrasting vermicomposting rate s between two worms: Eisenia foetida and a Native Worm. Tropical Ecology and Conservati on. 93-104. CIEE, Summer.
Lapied, E. and P. Lavelle. 2003. The peregrine eart hworm Pontoscolex corethrurus in the East coast of Costa Rica. The 7th 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 rationi ng. 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 Nonindigenous Earthworm Species. US Fish and Wildlife Service. UC Sustainable Agriculture Research and Education P rogram. 2008. Eisenia foetida (Savigny) (Lumbricidae).
APPENDIX I Morphospecies Three of the morphospecies I identified. Morphospecies pink-head : distinctive pink head, grey body, lighter-grey posterior (varied som e in darkness). Based on descriptions this may be Pontoscolex corethrurus Mller. Morphospecies: short, fat, grey: all grey body, d istinctive segmentation, lobed end. (cut in half by trowel) Morphospecies: Large, active, dark: long dark bod ies, thrash/jump about when disturbed in whiplike body 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