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Arthropod Diversity and Dynamics in Secondary Forests in the Jobos

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15 Ambientis 2017: 39-58.

Arthropod Diversity and Dynamics in Secondary Forests in the Jobos Bay Area, Salinas, Puerto Rico SM Encarnación-Rodríguez1,2, MF Barberena-Arias1,3 1School of Natural Sciences and Technology, Universidad del Turabo 2School of Medical Technology, University of Puerto Rico, Medical Science Campus. Corresponding author: [email protected] Abstract. Natural disasters and human activities are responsible for the loss of biodiversity in the Jobos Bay, Salinas. To assess how arthropod diversity was affected we used two sampling methods: active search and butterfly net. Data were collected during dry and wet seasons from 2011 to 2013. The specific study areas represent sequential stages of forest recovery: agricultural field, 5 y, 10y, 15y and 40y forests, and a reference forest: mangrove. In the laboratory, collected arthropods were counted and identified to order. A total of 4544 individuals were collected, that represent 22 orders. Of these, 9 were common to all areas, and 5 were unique to specific habitats. We found that abundance and richness of arthropods varied among habitats and seasons. The species composition of arthropods varied among habitats, specifically mangrove arthropods were significantly different from other habitats, arthropods in the agriculture area differed from the majority of other areas, and sequential stages of recovery had sequential similarity in species composition. These results suggest that the arthropod community is made up of common and unique species that are present yearlong or only in specific seasons. Furthermore, mangroves are unique habitats that harbor a specific arthropod community, while nearby forests in sequential stages of recovery harbor sub groups of associated arthropods. As a consequence, mangroves are sensitive areas that should be preserved because associated arthropods are absent from recovering areas and any loss in mangrove cover will negatively affect their survival. Key words: abundance, active search, butterfly net, mangroves, secondary forests

Resumen. Los desastres naturales y actividades humanas son responsables de la pérdida de biodiversidad en la Bahía de Jobos, Salinas. Para evaluar como la diversidad de artrópodos fue afectada en este lugar usamos dos métodos de muestreo: búsqueda activa y jama. La data fue recolectada durante estaciones húmedas y secas desde el 2011 al 2013. Las áreas de estudio especificas representan estadios secuenciales en la recuperación de bosques: campo agrícola, y bosques de 5, 10, 15 y 40 años, y uno de referencia: manglar. En el laboratorio, colectamos los artrópodos los cuales fueron contados e identificados según su orden. Un total de 4544 individuos fueron recolectados, los cuales se representaron entre 22 órdenes. De estos, 9 fueron comunes para todas las áreas, y 5 fueron únicos para hábitats específicos. Encontramos que la abundancia y riqueza de artrópodos variaba entre estaciones y hábitats, mientras que la composición de especies de artrópodos variaba entre hábitats, especialmente los artrópodos del manglar, los cuales fueron significativamente diferentes de los otros hábitats. Los artrópodos del campo agrícola diferían de las otras áreas, y los estadios secuenciales de recuperación tenían similitud secuencial en composición de especies. Estos resultados sugieren que la comunidad de artrópodos está hecha de especies únicas y comunes que se presentan todo el año o solo en estaciones específicas. Además, los manglares son hábitats únicos que albergan comunidades de artrópodos particulares, mientras que los bosques cercanos que están en etapas secuenciales de recuperación hospedan sub grupos asociados de artrópodos. Como consecuencia, los manglares son áreas sensitivas que deben ser preservadas porque los artrópodos asociados están ausentes en las áreas de recuperación y cualquier pérdida en la cobertura de los manglares va a afectar negativamente su sobrevivencia.

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Introduction Puerto Rico modern landscape includes a mosaic of vegetation patches in different successional stages intermixed with forest patches of typical vegetation (e.g. mangroves). Secondary forests are characterized by being dominated by few fast growing species in early stages of forest recovery, and slow growing species later on (Brown and Lugo 1990) where insect play a fundamental role due to their participation in many ecosystem processes (Didham et al. 1996). Secondary forests are home to a variety of flora and fauna that in turn provide habitat and resources for many organisms, such as arthropods. Terrestrial arthropods play an important role in forest recovery because they participate in processes such as pollination where bees move gametes from one flower to another, and decomposition where arthropods influence soil nutrient dynamics (Didham et al. 1996). In addition, coastal forest ecosystems, such as mangroves are also threatened by human activities, despite being tied to terrestrial, marine and freshwater ecosystems (Lugo 1999a), and providing ecosystem services such as coastal protection, control of erosion, habitat for fishery species (Barbier et al. in press), nutrient sink, sediment capture (Lugo 1999b) and ecosystem products such as wood for construction (e.g. wood for boats), food (e.g. vegetables, tea substitutes), combustion materials (e.g. charcoal), and textile (e.g. fabric dye) (Lugo 1999b). Also mangrove forests are habitat for many species, for example in Puerto Rico, migratory and residential birds use this habitat either for nesting or for feeding (Laboy et al. 2008), as well as threatened species such as carrucho, juey comun and langosta espinosa, and endangered species such as mariquita de Puerto Rico, palometa and pelicano pardo (JBNERR 2011). On the other hand, coastal ecosystems are very sensitive to changes in the environment due to anthropogenic and natural disturbances which pose a threat to these ecosystems. In particular in Puerto Rico, coastal areas, such as Jobos Bay, are facing potential sea level rise and anthropogenic pressures on the landward side because of urban/agriculture development. Changes in Puerto Rico’s economy during the last century have resulted in an increase in the amount of abandoned agricultural lands that regain vegetation cover through secondary succession resulting in a mosaic of patches in different successional stages (Ewel and Whitmore, 1973; Thomlinson et al., 1996). In Jobos Bay National Estuarine Research Reserve in Salinas, Puerto Rico, the reserve includes mangrove forests that are surrounded by lands that represent habitats in different stages of recovery. These situation provides an opportunity to study arthropod communities associated to successional forests, and to reference habitats such as mangroves. Specifically, we addressed the following two questions: 1. How does the abundance and richness of arthropods change during succession among habitats and seasons as compared to reference habitats? According to Barberena-Arias and Aide (2003) richness increase as vegetation recovers, and according to Garrison and Willig (1996) the rainy season triggers biological activity, as a consequence we expected abundance and richness to increase among sequential stages of vegetation recovery and in the wet season. 2. How does species composition of arthropods change during succession as compared to reference habitats? According to Barberena-Arias and Aide (2002), arthropod composition differed between early and late successional stages in a chronosequence of secondary forests, therefore we expected arthropod to follow a similar pattern. Methodology

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Study Site The Jobos Bay National Estuarine Research Reserve is located in Salinas, at the southern of Puerto Rico. According to Laboy et al. (2008), natural disasters and human activities have resulted in a significant loss of biodiversity in this natural reserve. Similar to Puerto Rico, the forests in this reserve have been disturbed by both natural events and human activities, resulting in protected forests inside the Reserve surrounded by patches of disturbed forests that are in different stages of recovery, and that are located outside just in the limit of the Reserve. Specifically, this study was conducted in six habitats, i.e. inactive agricultural field, <5 yr recovery habitat, ~10 yr recovery habitat, ~15 yr recovery habitat, >40 yr recovery forest, and mangrove. The agricultural field was a cleared forest where agriculture was previously practiced and eventually was abandoned while the <5 yr and ~10 yr habitats were dominated by grasses and herbaceous vegetation with some scattered woody shrubs. The ~15 yr habitat was purposely planted with young trees, and also had some herbaceous vegetation and shrubs. Spatially, the <5 yr, ~10 yr and ~15 yr were close, within <1 km apart. The >40 yr habitat was a closed forest in which the canopy and understory provide shade to a high proportion of the ground, and plant species included evergreens and semi-deciduous species able to grow in moist or dry climates. The mangrove represented a reference forest, these forests are periodically flooded, dominated by plant species mainly from the Avicenniaceae and Rhizophoraceae families (Macintsoh and Ashton 2002), have high soil salinity (Lugo 1980) and lack a closed canopy. Data Collection Arthropod collection was performed in the wet season (2011 and 2012) and dry season (2012 and 2013) for a total of two wet seasons and two dry seasons. During each season, each site was sampled once by using two methods: branch clipping and butterfly nets. In each habitat we collected five branch clipping and five butterfly nets for a total of 10 samples per habitat. For branch clipping, we walked randomly inside the specific habitat avoiding habitat edges, looking for tree branches with high abundance in arthropod. Each branch was placed inside a butterfly net to prevent escape of arthropods, and strongly shaken to force arthropods out of the branch. Carefully the branch was removed from the butterfly net and collected arthropods were placed in a labeled vial with alcohol. For butterfly net, we located a central point inside the specific habitat and walked away from the central point in a straight line for 20 steps. At each step the butterfly net was swept over the herbaceous vegetation. This procedure was repeated five times ensuring that the five straight lines were in opposing directions. Collected arthropods were placed in a labeled vial with alcohol. Using a dissecting microscope and a dissecting kit, every arthropod in the sample was placed in a petri dish . After identification, each organism was transferred into the flask. Arthropods were sorted, counted and identified to order using a dichotomous key. Data are expressed as number of individuals/sample. All the data was tabulated in a data worksheet. Data Analysis To determine differences in arthropod abundance due to habitat and season, a two-way ANOVA was used. Species composition was evaluated using orders as surrogates. To determine differences in arthropod composition among habitats, a Multi-Response Permutation Procedure (MRPP) was used, MRPP tested for differences in dissimilarity among predefined group (McCune and Grace 2002). MRPP used an arthropod abundance matrix where columns were arthropod Orders and rows were sampling units defined as samples taken in each year, in each habitat, for each of the two sampling methods and five replicates. Predefined groups were habitat and seasons.

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Results We found that arthropod abundance did not vary among habitats or seasons while richness significantly varied among habitats and seasons (Table 1). Arthropod abundance was highest in the inactive agricultural field (45±27 ind/sample) in the wet season and lowest in the ~10 yr habitat (7±2 ind/sample) in the dry season (Figure 1). Overall, there was a trend for higher arthropod abundance in the agricultural field, < 5 yr and ~10 yr habitats in the wet season, while abundance was higher in the dry season in the ~15 yr and >40 yr habitats and mangroves (Figure 1). On the other hand, richness was highest in the wet season in all habitats ranging between 4 to 7 Orders/sample, while in the dry season richness ranged between 3 to 5 Orders/sample. Table 1. ANOVA results for the effect of type of habitat (inactive agriculture, <5 yr, ~10 yr, ~15 yr, >40 yr forests, mangrove) and season (dry and wet) on arthropod abundance and Order richness. This experimental design included six habitats, two seasons (for two years), two sampling methods and five samples for a total of 240 samples.

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Figure 1. Average arthropod abundance (individuals/sample) (±s.e.) and average arthropod Order richness (number/sample) (±s.e.) in the dry and wet seasons in each of the six habitats. A total of 4,544 individual representing 22 Orders were collected in the 6 habitats (Table 2). Of these, 9 were common to all areas, and Acari, Araneae and Coleoptera were the most abundant, while 6 were unique to specific habitats, for example Diplopoda and Isopoda were unique to the ~15 yr habitat, Ephemeroptera to the agricultural field, Phasmida to the <5 yr habitat, Protura to the ~10 yr habitat and Pseudoscorpionida to the ~15 yr habitat. Acari and Coleoptera had significantly higher abundance in the agricultural field while Collembola was significantly more abundant in the <5 yr habitat. Table 2. Average arthropod abundance (±standard deviation) per Order in each of the six habitats. Lowercase letters indicate significant differences among habitats.

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Species composition based on Order identity was significantly different in the agricultural field and Mangrove, while the <5 yr, ~ 10 yr, ~ 15 yr, and >40 yr habitats showed a similar composition in sequential stages of forest recovery (Figure 2). For example, in Mangroves, Neuroptera was only collected in mangroves in the dry season 2012, while Isoptera was only collected in the wet season 2012 (Appendix 1). The sequential stages of forest recovery (i.e. < 5 yr, ~10 yr, ~15 yr and >40 yr habitats) had sub groups of associated arthropods among different areas (Appendix 1).

Figure 2. Species composition based on Order identity on habitats representing sequential stages of forest recovery, and reference habitats i.e. agricultural field and mangrove forest. Pvalues are indicated, the ‘~’ symbol indicates no significant difference in composition between consecutive habitats, and the ‘≠’ indicates a significant difference in order composition. Discussion In summary, this study found that although arthropod abundance was not significantly different, there was a trend for highest abundance in the inactive agricultural field, and also in the wet season. Also, Order richness was highest in the wet season in all habitats, and composition based on Orders was significantly different in the agricultural field and mangrove when compared to other habitats, and similar between sequential stages of forest recovery. Many studies have linked arthropod activity and abundance to rainfall, specifically reporting higher abundance and activity during the rainy season (Garrison and Willig 1996). In this study in the wet season, richness was significantly higher while there was a trend for higher abundance. These results corroborate previous findings that link arthropod diversity to water availability. Nevertheless, the >40 yr forest and mangrove had higher abundance during the dry season suggesting that arthropods associated to these typical habitats are adapted to drier conditions which may stimulate their activity Other studies have found higher arthropod abundance in habitats dominated by short vegetation (Barberena-Arias et al. 2012), such as pastures which lack tall trees and have high solar radiation (Barberena-Arias and Aide 2002). These open habitats are home to organisms associated to this kind of vegetation, for example Heteroptera include insects that are usually

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found in herbaceous/pasture vegetation (Borror et al. 1989), and were abundant in the agricultural field. The lack of trees also results in open habitats having higher temperature and lower humidity with larger daily fluctuations, as compared to closed habitats such as forests (Barberena-Arias et al. 2012). These combination of characteristics offer a particular set of resources and microclimate that harbor specific sets of associated arthropods adapted to this habitat, explaining the unique composition of arthropods in the agricultural field. Other studies have also found similar species composition in habitats with woody vegetation. For example, once a recovering habitat has growing trees, it offers similar resources and microclimate conditions despite variation in vegetation height, density and plant species composition (Barberena and Aide 2003, Osorio-Pérez et al. 2007). These characteristics result in similar sets of associated arthropods. The mixture of woody vegetation with shrubby vegetation, in addition to the spatial proximity of the <5 yr, ~10 yr and ~15 yr, probably facilitated arthropod movement among these habitats resulting in the similar composition in sequential stages of forest recovery, i.e. <5 yr, ~10 yr, ~15 yr and >40 yr habitats, found in this study. Mangroves represent a unique habitat with specific plant species and conditions (Macintsoh and Ashton 2002). For example, mangroves are dominated by plant species mainly belonging to Avicenniaceae and Rhizophoraceae (Macintsoh and Ashton 2002), have high temperature, salinity and humidity (Lugo 1980) that represent extreme conditions. In addition, terrestrial invertebrates are mangrove residential organisms (Macintsoh and Ashton 2002) that are adapted to the specific conditions that occur in this type of habitat. As a consequence, a unique set of associated organisms is expected to be found here such as the unique arthropod Order composition found in this study. The results of this study suggest that mangroves are unique habitats that harbor a specific arthropod community that should be preserved given that any loss in mangrove cover may result in loss of biodiversity. Nevertheless, these results are limited to the time span and used methodologies. To accurately assess arthropod communities, in particular communities that have been little studies, such as those associated to mangroves, a more extensive study including a variety of complementary methodologies, should be implemented. Acknowledgements We would like to thank the JBNERR staff for their logistic support during the field trips. We also thank Anivonne Robert, John González, Manuel Soler, Nohelysmarie Delgado, Juan Mendoza, Karen Ocasio, Linette Torres, Annette Torres, José Figueroa, Marielys Díaz, Gisel Ortíz and many others for their help during sample collection and processing. Universidad del Turabo provided logistic support. References Cited Barberena-Arias MF and TM Aide. 2003. Variation in species and trophic composition of insect communities in Puerto Rico. Biotropica 34(3): 357-367. Barberena-Arias MF and TM Aide. 2003. Species Diversity and Trophic Composition of Litter Insects during Plant Secondary Succession. Caribbean Journal of Science 39(2): 161– 169. Barberena-Arias MF, J Ortiz-Zayas, C Abad, G Almodóvar, E López, M Rodríguez, M Samó, G Davila, L Troche. 2012. Comparación de la fauna de artrópodos terrestres entre pastizales y bosques dominados por el tulipán africano, en tres zonas del karso norteño en Puerto Rico. Acta Cientifica 26 (1-3): 68-79.

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Barbier E, Hacker S, Kennedy C, Koch E, Stier A, Silliman B. in press. The value of estuarine and coastal ecosystem services. Ecological Monographs Borror DJ, CA Triplehorn, NF Johnson. 1989. An introduction to the study of insects. Saunders College Division. ISBN-10: 0030253977. Brown S and AE Lugo. 1990. Tropical secondary forests. Journal of Tropical Ecology 6(1): 132 Didham RK, J Ghazoul, NE Stork and AJ Davis. 1996. Insects in fragmented forests: a functional approach. TREE 11(6): 255-260. Ewel JJ and JL Whitmore. 1973. The Ecological Life Zones of Puerto Rico and the U.S. Virgin Islands. USDA Forest Service, Institute of Tropical Forestry, Research Paper ITF-018 Garrison RW and MR Willig. 1996. Arboreal invertebrates. In: The food web of a tropical rain forest: 183-246, eds. DP Reagan and RB Waide. The University of Chicago Press. Laboy EN, J Capellla, PO Robles and CM González. 2008. Jobos Bay Estuarine Profile – A National Estuarine Research Reserve. 118 pp. [JBNERR] Jobos Bay National Estuarine Research Reserve. 2011. Endangered and threatened species list. Aguirre, PR. http://ctp.uprm.edu/jobos/especies/ Lugo AE. 1980. Mangrove ecosystems: successional or steady state? Biotropica 12(2): 65-72. Lugo AE. 1999a. Mangrove ecosystem Research with emphasis on nutrient cycling. In: Ecosistemas de manglar en America Tropical, Eds. A Yañez-Arancibia, AL LaraDominguez. Instituto de Ecología, AC, Mexico, UICN/ORMA, Costa Rica, NOAA?NMFS Silver Spring MD USA. Lugo AE. 1999b. El manglar: un ecosistema al servicio del ser humano. Macintosh DJ and EC Ashton. 2002. A Review of Mangrove Biodiversity Conservation and Management. Centre for Tropical Ecosystems Research, University of Aarhus, Denmark (cenTER Aarhus). McCune B and JB Grace. 2002. Analysis of ecological communities. MjM Software Design, Gleneden Beach, Oregon. Osorio-Pérez K, Barberena-Arias MF and TM Aide. 2007. Changes in Ant Species Richness and Composition during Plant Secondary Succession in Puerto Rico. Caribbean Journal of Science 43(2): 244-253. Thomlinson JR, MI Serrano, TM Lopez, TM Aide and JK Zimmerman. 1996. Land-Use Dynamics in a Post-Agricultural Puerto Rican Landscape (1936-1988). Biotropica 28(4): 525-536.

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Appendix 1. Total abundance of arthropod Orders collected with each of the two sampling methods, in each of the six study habitats and for each sampling period. Numbers represent the sum of collected individuals in each of the five replicates. A1a.

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A1b.

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A1c.

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A1d.

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Arthropod Diversity and Dynamics in Secondary Forests in the Jobos

15 Ambientis 2017: 39-58. Arthropod Diversity and Dynamics in Secondary Forests in the Jobos Bay Area, Salinas, Puerto Rico SM Encarnación-Rodríguez1...

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