Typha Domingensis(Typhaceae) Affects Macroinvertebrate Assemblages in the Palo Verde Wetland

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The Management of Typha domingensis(Typhaceae) Affects Macroinvertebrate Assemblages in the Palo Verde Wetland...

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The user has requested enhancement of the downloaded file. The Management of Typha domingensis (Typhaceae) affects Macroinvertebrate Assemblages in the Palo Verde Wetland, Guanacaste, Costa Rica

Florencia A. Trama, Federico L.S. Rizo Patron Viale, Anjali S. Kumar, Jennifer L. Stynoski, Michael B. McCoy Colton, Monika C Springer

Ecological Restoration, Volume 35, Number 2, June 2017, pp. 175-189 (Article)

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The Management of Typha domingensis (Typhaceae) affects Macroinvertebrate Assemblages in the Palo Verde Wetland, Guanacaste, Costa Rica Florencia A. Trama, Federico L.S. Rizo Patron Viale, Anjali S. Kumar, Jennifer L. Stynoski, Michael B. McCoy Colton and Monika C. Springer

ABSTRACT The Palo Verde wetland, one of the most important places for aquatic organisms in Costa Rica, is currently recovering from an invasive expansion of Typha domingensis (cattail). A monitoring program was designed to understand the potential impacts of different management plans on aquatic fauna and flora. Macroinvertebrates were sampled monthly for one year (Aug 2003–Aug 2004) using an artificial substrate method in three plots: Plot A,T. domingensis has been managed since 1987 by manual and mechanical underwater cutting and posterior grazing; Plot B, T. domingensis has been mechanically crushed since 2002; and Plot C, a homogeneous T. domingensis stand without active management. We identified 112 macroinvertebrate taxa from 53 families and 18 orders. Typha domingensis removal in plots under active management did not increase family or taxa richness. Instead, a greater number of rare taxa persisted in the unmanaged plot, and macroinvertebrate communities differed among plots with less than 60% of taxa shared among them. Furthermore, mean taxa richness was higher in T. domingensis cover (X̅ = 8.56) than in the other vegetation covers (X̅ = 4.6 to 5.54). Macroinvertebrate richness was affected by vegetation cover, sampling date, and depth while abundance was affected by depth and dissolved oxygen. Typha domingensis management is necessary to open areas that allow the development of other vegetation types, a variety of communities of macroinvertebrates, and habitat for birds. However, in order to promote a high macroinvertebrates biodiversity and ensure food sources for waterfowl, the Palo Verde wetland should retain some patches of T. domingensis distributed throughout.

Keywords: aquatic diversity, cattail, seasonal wetland, tropical, wetland restoration

Restoration Recap • • Seasonally variable habitat conditions influence macroin- management activities to reduce invasive species stands, vertebrate communities. In this study, water depth was the importance of the invasive species as a habitat source one of the most important habitat factors aside from should be investigated. management activity. It is important to evaluate a range • Remnant cattail stands should be at least 15 m in diameter of both temporal and physical conditions in a system in to ensure a low electric conductivity needed to sustain a order to achieve restoration goals. diverse macroinvertebrate community. • Macroinvertebrates can adapt to live on invasive plants that have been established for a long time. Before starting

reshwater wetlands are the most threatened ecosystems (Bufford and Gonzalez 2012). These threats are mainly Fin the world and provide critical habitat for a variety of due to direct activities (drainage, dredging, and dam- organisms, including birds, fish, amphibians, and reptiles ming) that modify the land for agriculture, ranching and aquaculture among others. Additionally, water pollutants, Ecological Restoration Vol. 35, No. 2, 2017 excess of nutrients, and the introduction of non-native ISSN 1522-4740 E-ISSN 1543-4079 species by natural dispersal mechanisms or human trans- ©2017 by the Board of Regents of the University of Wisconsin System. portation have changed community structure and wetland

June 2017 ECOLOGICAL RESTORATION 35:2 • 175 functionality (Roggeri 1995, Cronk and Fennessy 2001, was developed by the Ministry of Environment, Energy Ramsar 2014). and Telecommunications (MINAET; Castillo and Guzmán Non-native invasive plants can be successful due to 2004) and the Organization for Tropical Studies (OTS). their ability to rapidly adapt and spread with both sexual The project included a component for monitoring the reproduction and vegetative regeneration. Invasive plants responses of wetland fauna and flora to various methods often have wide ecological tolerances to fire, flooding and of controlling T. domingensis (Organization for Tropical drought conditions, and often do not have pests or herbi- Studies 2002, Trama and Rizo-Patron 2007, Trama et al. vores in the new, invaded habitats (Cronk and Fennessy 2009a, Trama et al. 2009b). 2001). These invasions not only affect the associated bio- Macroinvertebrates play an important role in the food diversity but also the functionality of the ecosystems and web and recycling of organic matter. These organisms human interests (Zedler and Kercher 2004). Some of the are an important source of protein for many aquatic changes that can be observed when an invasive plant arrives species, including birds that forage and nest in wetland to a new wetland are: 1) changes in community structure areas (Fredrickson and Reed 1988). Generally, there are a by competition and habitat disturbance; 2) changes in greater number of macroinvertebrates found in wetlands aquatic plant composition by shading the water column; with aquatic vegetation than in those without vegetation 3) producing more invasive hybrids that change the genetic (Kostecke et al. 2005). Moreover, areas with a greater makeup of the community; and 4) changes in animal com- diversity of wetland vegetation structures support a more munities by modifying the physicochemical factors or diverse assemblage of macroinvertebrates than areas with biotic conditions (Cronk and Fennessy 2001). one or few plant species (De Szalay and Resch 2000, Kratzer Palo Verde National Park (PVNP; Guanacaste, Costa and Batzer 2007). Rica) includes a 1247-hectare (ha) seasonal, freshwater Traditionally, wetland managers have manipulated wetland (Palo Verde wetland, PVW), considered one of the hydrology and vegetation to benefit waterfowl populations, most important wetlands in the Pacific region of Central especially migratory birds. However, some management America (Vaughan et al. 1996). This wetland provides vital activities have shifted to also benefit macroinvertebrates habitat for over 60 species of migratory and resident water because they act as a food source for waterfowl (De Szalay birds (Boza 1981, Boza and Mendoza 1981, McCoy and et al. 1996, De Szalay and Resh 1997, Kostecke 2005). Cur- Rodríguez 1994), including endangered species and those rently, no information is available regarding the impacts with small population sizes (Vaughan et al. 1996). Since of T. domingensis management on macroinvertebrates in the 1980s, when PVNP was created and grazing cattle were the PVW. Here, we investigated the responses of mac- removed, the aggressive advance of Typha domingensis roinvertebrate communities to T. domingensis manage- (cattail) and other grasses have made the maintenance ment methods to determine how richness and abundance of aquatic habitat for organisms difficult (McCoy and of food for resident and migratory birds may be altered Rodriguez 1994). (Gray et al. 1999, Camburn et al. 2001, Kostecke et al. Typha domingensis is a cosmopolitan plant distributed 2005). Our objectives were to compare throughout the in the Americas, Africa, and Australia (Sojda and Solberg year: 1) diversity of aquatic macroinvertebrates in differ- 1993). In Costa Rica, this species has shown very aggres- ent T. domingensis management treatments; 2) variation sive growth in many wetlands, including those found in of physicochemical measures between treatments; and the lower reaches of the Tempisque River (Organization 3) the relationship between biodiversity (biotic) variables for Tropical Studies 2002, Jiménez et al. 2003, Organiza- and physicochemical (abiotic) variables. tion for Tropical Studies 2003, Castillo and Guzmán 2004, Pucci 2012). Several methods have been employed and Methods tested in an effort to control the growth of this plant and restore natural wetlands (McCoy 1994, McCoy and Rodrí- Study Area guez 1994, McCoy 1996, Vaughan et al. 1996). However, The Palo Verde wetland is situated within the Palo Verde T. domingensis grows very quickly in wetlands due to its National Park (10°20'35" N, 85°20' 26" W) in the province clonal growth strategy and produces an inflorescence with of Guanacaste, Costa Rica (Figure 1). The marsh has a sea- about 250,000 seeds that can remain viable for up to 100 sonal regime, filling mostly with rainwater runoff from the years (Sojda and Solberg 1993). surrounding hills during the rainy season and drying via Currently, active management of T. domingensis in the evapotranspiration during the dry season. Water depth in Palo Verde wetland is performed by a technique adapted the marsh ranges from 0 to 1.5 m in the rainy season (May from the irrigated rice cultivation called “fangueo”, which to November) and 0 to 40 cm in the dry season (Decem- uses a tractor with padded iron wheels that crush T. domin- ber to April), and it is completely dry between late March gensis underwater and inhibit oxygen conduction to the and mid April (Vaughan et al. 1982, Vaughan et al. 1996, roots (Trama 2005). In 2002, a massive restoration project Calvo and Arias 2003). Seven general types of vegetation

176 • June 2017 ECOLOGICAL RESTORATION 35:2 Figure 1. Location of management plots (A, B, C) in the Palo Verde wetland (in gray), Guanacaste, Costa Rica. coverage/habitat can be found in the wetland: floating Typha domingensis Management vegetation, emergent vegetation, Parkinsonia aculeata (Palo Management activities with a fangueo and tractor were Verde trees), T. domingensis, crushed T. domingensis, bodies applied in Plots A and B from July 2002 to April 2004, of water, and exposed soil (Plot 2005). including the period of this study (Trama 2005). In July Palo Verde Wetland Management History 2002, about 35 ha of T. domingensis were crushed in Plot A in areas that had been managed historically. In September This study focuses on three contiguous management plots 2002, crushing began in Plot B and continued into the dry of 80 ha each (Figure 1) established in 2002. Until they season of 2003. Crushing was not completely successful were removed in 1970, grazing cattle controlled T. domin- due to low water depth (< 45 cm) in the marsh. A second gensis and other aquatic grasses in all three plots, and in crushing was conducted in the dry season of 2004 (May), 1980, T. domingensis invaded much of the wetland. When but was preceded by a controlled burn to reduce the bio- established in 2002, Plot A had six different habitat types mass of T. domingensis and in this second case, crushing due to historical management of 36 of 80 ha, including by tractor was completed more rapidly. In Plot C, no underwater cutting with machete and manual or mechani- management activities were performed, and a large area cal cutters in 1989 as well as crushing in 1990. The aquatic of T. domingensis and some small areas of P. aculeata were vegetation and water bodies present in those 36 ha in Plot A present. Crushing methodology and resulting changes in reflected the conditions present in the wetland for decades plant coverage in managed plots are outlined in Trama et before the invasion of T. domingensis (Trama et al. 2009a). al. (2009a). Before treatment in 2002, T. domingensis dominated both Plot B (62%) and Plot C (66%; McCoy and Rodríguez 1994, Aquatic Macroinvertebrate Sampling Trama 2005). Except for P. aculeata and T. domingensis, Macroinvertebrate collection was performed monthly which remain in the wetland even when completely dry, between August 2003 and August 2004, with the excep- the other vegetation types appear as the marsh begins to tion of April-June 2004 when the marsh was completely fill in the rainy season and occupy different areas according dry, with a total of ten sampling events during the study. to the depth of water in each location (Trama et al. 2009a). We used the artificial substrate method, allowing the

June 2017 ECOLOGICAL RESTORATION 35:2 • 177 colonization of macroinvertebrates for one month at a Analysis of Variance (ANOVA). Additionally, differences time. Each substrate consisted of a concrete block (20 × 12 between vegetation cover and season (dry and wet) for × 5 cm) inside a plastic mesh bag (0.5 cm mesh size). Two “taxa richness” and “abundance” response variables were substrates were placed at each sampling station (Castillo estimated using ANOVAs. Differences between each physi- 2000, Trama et al. 2009b). Nine sampling stations, three cochemical variable between plots and sampling dates were in each plot, were randomly distributed at the beginning assessed using a parametric multifactor ANOVA. For all of the project, including areas of the marsh with differ- analyses, the data from April to June of 2004 was excluded ent depths and types of coverage. All sampling stations because the wetland was completely dry. Our final sample were sampled every 30 days, with a sampling effort of 18 size was 10 months. Assumptions of normality and homo- blocks per month for a total of 180 blocks. All the sampling geneity of variance were always tested before proceeding stations were sampled on the same day. with parametric ANOVAs and Post hoc comparisons of To collect macroinvertebrates, both the blocks and bags means were performed using Tukey tests (Sokal and Rohlf were washed in a bucket and the collected sample was 1995). filtered through a 500μm sieve, and then preserved in We also performed two multivariate analyses with rich- 90% ethanol. The blocks were returned to the field after ness and abundance response variables separately using being washed. Macroinvertebrates were preserved in 70% a linear model against the biotic (vegetation cover) and ethanol and identified to the finest taxonomic level pos- abiotic (five physical-chemical variables as well as sampling sible, whether species (some cases), genus (most cases) or date, season, and plot) variables. Finally, for each model, the family (Roldán 1988, Roldán 1999, Springer 2006). “Taxa” statistical value of Wilk’s lambda for multivariate ANOVA is defined as the total number of finest taxonomic levels (MANOVA) was calculated to determine the effect size of identified for a given sample (coarser levels, families or each independent variable on the dependent variable. All genera, were not counted if a finer level was identified). analyzes were performed with Statgraphics Centurion XVI In addition, physicochemical variables were measured (StatPoint Technologies, Warrenton, VA). in the field at three points (replicates) near each sampling station and during each sample date. Temperature (c), Results electric conductivity (μs/cm), pH, and dissolved oxygen (mg/L) were measured with a field meter (YSI80) and Macroinvertebrate Richness depth (m) was measured with a ruler. We calculated the We found a total richness of 112 taxa belonging to five mean values for each variable at every sampling event for orders and 18 families (Table 1). The total macroinverte- further analysis. Macroinvertebrates were deposited at both brate taxa richness was similar in plots B (82) and C (81), the Palo Verde Biological Station and Aquatic Entomology and higher in both of those cases than in plot A (74). Collection of the Museum of Zoology, University of Costa However, 23 rare taxa were found in only one of the Plots Rica (MZUCR). Data Analysis and Measures of Diversity The mean taxa richness and macroinvertebrate abundance were estimated per Plot (A, B, or C). Classification of abundance was established according to the following: Rare or I, 1 individual; Occasional or II, 2–10 individuals; Frequent or III, 11–50 individuals; and Abundant or IV, > 50 individuals (Trama et al. 2009b). Taxa accumulation curves were created for each plot sample (summing repli- cas) with the estimate of abundance-based coverage (ACE) (Colwell 2013) in the program EstimateS 8.20 to determine the theoretical number of taxa that should have been collected in each plot (Espinosa 2003). Shannon-Wiener diversity indices were estimated for each plot, first by summing all samples of the entire study and second by using mean values for each sampling event. We also assessed the Figure 2. Taxa accumulation curve according to Abun- Jaccard similarity index for pairwise combinations among dance Estimator based on coverage (ACE) for each plot the three plots (Moreno 2001). (closed circles-Plot A, open circles-Plot B and triangles- For each biodiversity response variable (macroinver- Plot C) and number of blocks (six blocks of each plot tebrate taxa richness and abundance), differences among are combined for each plot/sampling date) in the Palo the three plots and 10 sampling dates were estimated using Verde wetland.

178 • June 2017 ECOLOGICAL RESTORATION 35:2 Table 1. Collected macroinvertebrates in the Palo Verde wetland (Guanacaste, Costa Rica) for each management plot. Abundance classification for each taxa: rare or I, 1 individual; occasional or II, 2–10 individuals; frequent or III, 11–50 individuals; and abundant or IV, > 50 individuals (Trama et al. 2009b).

Plot A Plot B Plot C Abundance Abundance Abundance Taxa # Individuals class # Individuals class # Individuals class Oligochaeta 35 III 2 II 116 IV Hirudinea 17 III 93 IV 28 III Mollusca Basommatophora Bulinidae Gundlachia radiata 1 I Lymnaeidae 1 I 1 I 2 II Physidae 103 IV 131 IV 235 IV Planorbiidae Planorbella sp. 81 IV 34 III 21 III Biomphalaria sp. 4 II 2 II Antillorbis aeruginosus 35 III 10 II 39 III Drepanotrema anatinum 119 IV 60 IV 75 IV Mesogastropoda Ampullariidae/Pilidae Pomacea flagellata 12 III 8 II 9 II Hydrobiidae Aroapyrgus costaricensis 2 II 12 III Thiaridae Melanoides tuberculata 1 I 2 II 7 II Veneroidea Sphaeriidae Eupera veatleyi 19 III Collembola sp. 1 2 II 2 II 7 II Insecta Ephemeroptera Baetidae Baetis sp. 5 II Callibaetis sp. 1 I Fallceon sp. 14 III Polymitarcidae Campsurus sp. 1 I Caenidae Caenis sp. 5 II 376 IV Leptohyphidae Leptohyphes sp. 3 II 4 II Leptophlebiidae Farrodes sp. 2 II Traverella sp. 1 I Megaloptera Corydalidae Corydalus sp. 1 I Hemiptera Hydrometridae Hydrometra sp. 1 I Belostomatidae Lethocerus sp. 1 I 11 III Hebridae Hebrus sp. 16 III 6 II 24 III

June 2017 ECOLOGICAL RESTORATION 35:2 • 179 Table 1., continued

Plot A Plot B Plot C Abundance Abundance Abundance Taxa # Individuals class # Individuals class # Individuals class sp.1 1 I Veliidae Microvelia sp. 1 I sp. 1 1 I Mesoveliidae Mesovelia sp. 11 III 3 II 5 II Naucoridae Pelocoris sp. 5 II 2 II Notonectidae Buenoa sp. 1 I 2 II Pleidae 5 II 7 II 32 III Corixidae 2 II Nepidae Curicta sp. 1 I Ranatra sp. 3 II Odonata Libellulidae Anatya sp. 1 I Erythemis sp. 5 II 1 I 2 II Erythemis vesiculosa 3 II Orthemis sp. 1 I 7 II 1 I Pantala sp. 3 II 4 II 1 I Perithemis sp. 8 II 23 III 1 I Tramea sp. 11 III Pseudoleon sp. 1 I Nephepeltia sp. 2 II 2 II 6 II Miathyria sp. 1 I 1 I 3 II sp 1. 2 II 1 I 2 II sp.2 1 I 1 I sp.3 2 II Aeshnidae Anax sp. 1 I 1 I 14 III Calopterygidae Heteaerina sp. 1 I Coenagrionidae Ischnura ramburii 6 II Telebasis sp. 6 II Leptobasis sp. 23 III Acanthagrion sp. 2 II 7 II 10 II Argia sp. 3 II 11 III Coleoptera Elmidae Microcylloepus sp. 1 I 2 II Haliplidae Haliplus sp. 2 II Staphylinidae 3 II Lampyridae sp. 1 1 I Lutrochidae 1 I sp. 1 1 I Dryopidae Pelonomus sp. 1 I

180 • June 2017 ECOLOGICAL RESTORATION 35:2 Table 1., continued

Plot A Plot B Plot C Abundance Abundance Abundance Taxa # Individuals class # Individuals class # Individuals class Dytiscidae sp.1 10 II 1 I 7 II sp.2 4 II 2 II 4 II sp.3 3 II 2 II 17 III sp.4 1 I 1 I 1 I Noteridae sp.1 2 II 10 II 12 III sp.2 1 I 2 II 14 III Hydrophilidae Derallus sp. 3 II 1 I 70 IV Berosus sp. 15 III 16 III 49 III Tropisternus sp. 4 II Helochares sp. 1 I 7 II Phaenonotum sp. 1 I 1 I 4 II Hydrophilus sp. 7 II Helobata sp. 8 II 1 I Enochrus sp. 5 II 2 II 1 I sp. 1 3 II 1 I 8 II Scirtidae 12 III 8 II 220 IV Curculionidae 2 II Trichoptera Hydropsychidae Smicridea sp. 1 I Hydroptilidae Hydroptila sp. 1 I 9 II 1 I Neotrichia sp. 4 II 10 II 2 II Oxyethira sp. 144 IV 1 I Leptoceridae Nectopsyche sp. 6 II Oecetis sp. 1 I Lepidoptera Crambidae Petrophila sp. 1 I Diptera Ceratopogonidae Probezzia sp. 7 II 2 II Alluaudomya sp. 3 II 1 I sp.1 3 II 3 II 5 II Chironomidae Tanypodinae 35 III 147 IV 26 III Podonominae 1 I 2 II Chironominae 381 IV 772 IV 337 IV Tabanidae Chrysops sp. 6 II 4 II 3 II Tabanus sp. 1 I Culicidae Aedeomyia squamipennis 1 I Culex culex 4 II Culex erraticus 1 I Mansonia dyari 12 III Mansonia titillans 3 II Chaoboridae

June 2017 ECOLOGICAL RESTORATION 35:2 • 181 Table 1., continued

Plot A Plot B Plot C Abundance Abundance Abundance Taxa # Individuals class # Individuals class # Individuals class Chaoborus sp. 1 I Stratiomyidae 23 III 2 II 20 III Tipulidae sp 1. 1 I 1 I Tipula sp. 1 I 1 I Arachnoidea Acari/acarina Fam. Indet. 10 II 2 II 1 I Oribatidae 10 II Crustacea Conchostraca 35 III 1752 IV 1 I Cladocera Daphniidae 5 II 24 III 6 II Ostracoda Cyprididae Zonocypris sp. 2 II Sasrcypridopsis sp. 12 III 3 II 1 I Lymnocytheridae Cytheridella sp. 11 III 244 IV 83 IV Gen. sp. 1 18 III 129 IV 9 II Gen. sp. 2 38 III 27 III 149 IV Gen. sp. 3 2 II 104 IV 7 II Gen. sp. 4 4 II 9 II 20 III Gen. sp. 5 1 I 12 III Gen. sp. 6 5 II 4 II 1 I

Family richness per plot 35 39 40 Total Family richness (entire study) 53 Taxa richness per plot 74 82 81 Total Taxa richness (entire study) 116 Individual abundance per plot 1186 4317 1848 Total Individual abundance 7351 (entire study) and not in the other two. The number of taxa increased The Shannon diversity index for the entire study (com- as sampling progressed (Figure 2), and new taxa were bining all samples) was 3.50 for Plot A, 2.65 for B, and 3.66 present even in the last sampling. The ACE estimator of for C. The Shannon diversity index when averaged across theoretical richness suggested 90 taxa for Plot A, 113 for sampling efforts was 2.17 for plot A, 1.90 for B, and 2.33 for B, and 103 for Plot C. C, with no significant difference between plots (Multifactor Mean taxa richness was higher in plot C (X̅ = 7.7) than ANOVA; F 2,180 = 0.74, p = 0.4849). The Jaccard similarity in plots A and B (both X̅ = 5.1) (Multifactor ANOVA; index showed similarity values of 58% between plots A F 2,180 = 3.75, p = 0.0254; Figure 3A). Additionally, mean and B, 57% between A and C, and 57% between B and C. richness varied according to the sampling date (Multifac- Abundance of Macroinvertebrates tor ANOVA F 9,180 = 6.96, p = 0.0013; Figure 3B), where the values for all three plots began lower in August 2003, We counted a total abundance of 1186 individuals in Plot increased through the rainy season, fell sharply in the dry A, 4317 in Plot B, and 1848 in Plot C. In all plots, the season and increased again in July 2004. Taxa richness organisms classified as abundant (level IV) were in the in plot C increased significantly more than in the other groups Hirudinea, Physidae, Planorbidae (Drepanotrema plots at the end of the study. In contrast, mean taxa rich- anatinum), Caenidae (Caenis sp.), Hydrophilidae (Derralus ness of macroinvertebrates in all plots was not different sp.), Scirtidae, Chironomidae (Tanypodinae and Chinoro- between the wet season (X̅ = 4.9) and dry season (X̅ = 5.2) minae), Conchostraca, and Ostracoda (Lymnocytheridae; (Multifactor ANOVA; F 1,180 = 0.09, p = 0.7680). Table 1).

182 • June 2017 ECOLOGICAL RESTORATION 35:2 Figure 3. Mean values and interaction patterns for each plot and sampling date in the Palo Verde wetland, August 2003–2004. A) Taxa Richness per plot, B) Taxa Richness per sampling date, C) Macroinvertebrate abundance per plot, D) Macroinvertebrate abundance per sampling date.

Mean macroinvertebrate abundance was higher in Plot (X̅ = 4.0), or open water (X̅ = 4.61; Multifactor ANOVA; B (X̅ = 71.8) than in Plot C (X̅ = 30.9) or Plot A (X̅ = 19.7; F 4,180 = 4.06, p < 0.0036). However, mean abundance of Multifactor ANOVA; F 2,180 = 7.04, p = 0.0012; Figure 3C), macroinvertebrates was not significantly different between and varied throughout the year (Multifactor ANOVA; vegetation cover types (Multifactor ANOVA; F 4,180 = 1.71, F 9,180 = 5.06, p < 0.00001) with a sharp increase in mean p = 0.15). abundance in Plot B in January-February (Figure 3D). Overall, mean abundance did not differ between the dry Physicochemical Variables in Each Plot season (X̅ = 49.6) and the wet season (X̅ = 31.9; Multifactor and During the Annual Cycle. ANOVA; F 1,180 = 1.52, p < 0. 2195). Mean dissolved oxygen was higher in Plot B (X̅ = 3.08) than in Plot A (X̅ = 2.01), and lower in Plot C (X̅ = 1.38; Macroinvertebrate Assemblage Structure Multifactor ANOVA; F 2,141 = 25.14, p < 0.00001). Mean Throughout the study, insects were the most diverse taxa dissolved oxygen levels were relatively constant throughout with a richness of 41 families, 62 genera, and 90 species the year with differences between September X( ̅ = 1.09) as compared to non-insect macroinvertebrates (Mollusca, and March (X̅ = 3.75; Multifactor ANOVA; F 9,141 = 5.19, Crustacea, Oligochaeta, and Hirudinea) with 14 families, p < 0.0001) as well as between the dry season (X̅ = 2.80) 12 genera, and 26 species (Table 1). Taxa richness of Cole- and the wet season (X̅ = 1.50; Multifactor ANOVA; F1,141 = optera was high in all three plots, as were Diptera in plot 24.01, p < 0.00001). A and Odonata in plots B and C (Table 2). The abundance Mean electric conductivity was higher in Plot A (X̅ = of Conchostraca represented over half of the individuals 705.6) and Plot B (X̅ = 673.3) than in Plot C (X̅ = 558.6; collected in plot B, whereas Diptera, Basomatophora, or Multifactor ANOVA; F2,141 = 5.36, p < 0.0058). Addition- Coleoptera had higher abundance in plots A and C (Table ally, conductivity varied over the sampling year (Multi- 2). Also, there were 7 unique taxa in plot A, 16 unique taxa factor ANOVA; F9,141 = 47.63, p < 0.0001), especially in in plot B, and 11 unique taxa in plot C (Table 1). August 2003 (X̅ = 565.90) versus August 2004 (X̅ = 1332.5). Conductivity was lower in the dry season (X̅ = 397.9) than Macroinvertebrates and Vegetation Cover in the wet season (X̅ = 666.3; Multifactor ANOVA; F1,141 Mean taxa richness of macroinvertebrates was higher in = 11.82, p < 0.00008). T. domingensis cover (X̅ = 8.56) than in emergent vegeta- Mean water depth was higher in Plots A and B (both with tion (X̅ = 5.41), floating vegetation X( ̅ = 5.54), exposed soil X̅ = 0.64) than in Plot C (X̅ = 0.57; Multifactor ANOVA;

June 2017 ECOLOGICAL RESTORATION 35:2 • 183 Table 2. Taxa richness and abundance of macroinvertebrates in % for each Class/Order collected in all sampling points.

Class /Order Plot A Plot B Plot C Taxa richness Oligochaeta 1.35 1.22 1.22 Hirudinea 1.35 1.22 1.22 Basommatophora 8.11 8.54 7.32 Mesogastropoda 2.70 3.66 3.66 Veneroidea — — 1.22 Ephemeroptera 5.41 7.32 — Trichoptera 4.05 6.10 3.66 Odonata 13.51 20.73 15.85 Coleoptera 20.29 18.29 24.80 Collembola — 1.22 1.22 Hemiptera 8.11 6.10 13.41 Lepidoptera — — 1.22 Diptera 18.92 10.96 10.98 Ostracoda 10.81 9.76 9.76 Acari/acarina 1.35 1.22 2.44 Cladocera 1.35 1.22 1.22 Conchostraca 1.35 1.22 1.22 Macroinvertebrate abundance Oligochaeta 3.57 0.21 6.54 Hirudinea 4.33 3.96 3.34 Basommatophora 26.03 4.22 18.25 Mesogastropoda 0.99 0.21 1.37 Veneroidea — — 0.93 Ephemeroptera 0.82 4.86 4.86 Trichoptera 0.46 3.00 0.20 Odonata 1.97 1.71 3.39 Coleoptera 5.31 0.90 21.44 Collembola 0.91 0.21 1.18 Hemiptera 3.04 0.32 4.02 Lepidoptera — — 0.05 Diptera 36.50 16.46 19.48 Ostracoda 6.38 9.20 13.83 Acari/acarina 0.76 0.04 0.54 Cladocera 0.38 0.42 0.29 Conchostraca 7.97 52.02 0.29

F2,141 = 6.55, p < 0.0019). Mean depth was higher during Mean pH differed between Plots B (X̅ = 6.79) and C the rainy season (X̅ = 1.1) and went down as the dry season (X̅ = 6.64), but not A (X̅ = 6.72; Multifactor ANOVA; progressed (X̅ = 0.3; Multifactor ANOVA; F9,141 = 74.14, F2,141 = 5.65, p = 0.0044). Across the year, pH was relatively p = 0.00001). Depth was lower in the dry season (X̅ = 0.53) constant from August to January (X̅ = 6.5–6.6) and then than in the wet season (X̅ = 0.74; Multifactor ANOVA; increased during the dry season (X̅ = 7.4; Multifactor F1,141 = 14.73, p < 0.0002). ANOVA; F9,141 = 21.35, p = 0.00001). However, pH was Mean temperature was higher in Plot B (X̅ = 29.89) not significantly different between seasons (Multifactor than Plot A (X̅ = 28.90) and Plot C (X̅ = 27.60; Multifactor ANOVA; F1,141 = 1.22, p = 0.2717). ANOVA; F2,141 = 26.79, p < 0.00001). Additionally, mean temperature varied over time and increased from August Multivariate analysis (X̅ = 27.91) to October (X̅ = 31.2), but fell sharply in The fit of taxa richness to a linear model was strong (Linear January (X̅ = 25.6) and then increased again in August (X̅ Model; F6,144 = 19.93, p < 0.00001, R2 = 0.466) with three = 30.3; Multifactor ANOVA; F9,141 = 23.67, p = 0.00001). predictive independent variables: vegetation cover (Linear Temperature was lower in the dry season (X̅ = 27.32) than Model; F4,144 = 4.14, p < 0.0034), sampling date (Linear in the wet season (X̅ = 30.13; Multifactor ANOVA; F1,141 Model; F1,144 = 16.41, p < 0.0001), and depth (Linear Model; = 57.97, p < 0.00001). F1,144 = 11.53, p = 0.0009; Figure 4A). The other predictor

184 • June 2017 ECOLOGICAL RESTORATION 35:2 variables (dissolved oxygen, conductivity, temperature, pH, season, and plot) were not significant in the model. The fit of macroinvertebrate abundance to a linear model was strong (Linear Model; F2,144 = 18.78, p < 0.0001, R2 = 0.212) with two predictive independent variables: dissolved oxygen (Linear Model; F1,144 = 16.50, p < 0.0001) and depth (Linear Model; F1,144 = 12.95, p < 0.0004; Figure 4B). The remaining predictor variables were not significant in the model.

Discussion Since 1980, T. domingensis has been expanding over the Palo Verde wetland. Water surface and vegetation cover has declined each year since grazing by cows has been halted (McCoy 1994, McCoy and Rodríguez 1994, Trama 2004, Trama et al. 2009b). The principal aim of the restoration project in the Palo Verde wetland was to open up areas of the marsh to recuperate populations of migratory and resident waterfowl (Organization for Tropical Studies 2002). Due to the importance of macroinvertebrates for recycling organic matter and as a food source for many aquatic and terrestrial species, both macroinvertebrates and birds have been the main subjects of the proposed monitoring project for the Palo Verde wetland restoration (Bambaradeniya 2000, Bambaradeniya and Amarasinghe 2003). Figure 4. Estimated surface responses for the adjust- Removal of Typha domingensis Does Not ment of: A) Taxa richness (vegetation cover = T. domingensis) and B) Abundance of macroinvertebrates to a Increase Macroinvertebrate Richness linear model (LM) versus the significant independent Contrary to our predictions, the results of this study variables (depth, dissolved oxygen, sampling date, and indicate that T. domingensis management in Plots A and vegetation cover). B did not favor an increase in total richness of macroinvertebrate taxa as compared to the control. This is possible than an excess of disturbance reduces the diver- evidenced by the following: 1) the control treatment had sity of macroinvertebrates in the assemblages in the active higher values of taxa richness, (totals and means); 2) the management plots. Also, emergent vegetation, such as mean and total values of Shannon-Wiener diversity indi- T. domingensis, may shade the water from direct sunlight ces were higher in control than in managed plots; 3) the and reduce water temperature, which can be a limitation prediction of the ACE index (expected taxa richness) was to some taxa (Molnár et al. 2011). lower for Plot A (with historical management since 1989) than for Plots C (without fangueo management-control More Unique Taxa in Control Plot plot) or B (with fangueo management since 2002); and Crushing appears to have influenced the structure and 4) a greater abundance for most orders was identified in composition of macroinvertebrate assemblages. There the control plot. were different exclusive taxa in the three plots. Crushing We identified a greater diversity of aquatic insects inside and subsequent decomposition of T. domingensis seem T. domingensis than in other habitats including emergent to have promoted an increase in the abundance of some vegetation and floating vegetation (Camburn et al. 2001, macroinvertebrates in Plot B. The most abundant groups van Duinen 2003). Our findings are consistent with those (Category IV) were Conchostracans, Chironominae, gas- of a study in a wetland in Kansas (USA) with active res- tropods and Caenis sp., with hundreds or thousands of toration (burning, disking, and grazing), in which greater individuals each. As Kostecke et al. (2005) mentioned, a diversity, biomass, and density of macroinvertebrates were greater structural complexity of habitat due to the presence observed in areas without management of T. domingen- of higher biomass and density of aquatic vegetation can sis (Kostecke et al. 2005). Some macroinvertebrates are encourage greater richness of taxa and greater abundance sensitive to disturbance (Kostecke et al. 2005, Merritt of each order present, which may be absent from areas with and Cummins 1996a, Cummins and Merrit 2001). It is strong disturbances.

June 2017 ECOLOGICAL RESTORATION 35:2 • 185 Removal of sediments by the tractor or cattle could 2003) (Trama et al. 2009b). Conchostracans have parthe- have altered the habitat, causing unequal establishment of nogenetic and asexual reproductive strategies, which help macroinvertebrate groups. In an assessment of suspended to increase populations very quickly. They also have eggs solids in a related species, T. angustifolia, the concentra- resistant to drought periods, so colonization can start as tion of suspended solids and the rate of re-suspension fast as the marsh fills with water and adults do not need of sediments were significantly lower within stands than to recolonize after each dry season (Pennak 1989, Thorp on the edge or outside of vegetation cover (Horppila and and Covich 2001). Nurminen 2001, Martin and Neely 2001). An increase in Ostracoda are considered one of the more abundant suspended solids and turbidity affects nutrient cycles and taxa of meiobenthos (Dole-Olivier et al. 2000), and in our primary productivity, negatively influencing the structure study these mollusks were dominant with abundances in and composition of the macroinvertebrate assemblages categories III and IV throughout the year. This group was and increasing predation by other species (Tallberg et most abundant in the summer of 2003 when the marsh al. 1999). is shallower, and in July 2004 when the marsh began to fill with rainwater (Trama 2005). Like Conchostracans, Macroinvertebrate Abundance and Seasonality Ostracod eggs remain dormant and can begin growing The Palo Verde wetland has a seasonal regimen and short- when the rainy season starts, which is an advantage over term hydrological changes likely determine the occur- other macroinvertebrates that are dependent on adults to rence and abundance of macroinvertebrates. Flooding re-colonize the wetland (Dole-Olivier et al. 2000). Several has been shown to affect the appearance, growth, survival species of gastropods bury into the mud, aestivating during and reproduction of macroinvertebrates (Margalef 1983, the summer period, and can return up to the surface when Fredrickson and Reed 1988). Seasonal growth of mac- the conditions are optimal (Pennak 1989). roinvertebrates assemblages occurs with the beginning of the rains in May each year in the Palo Verde wetland Macroinvertebrates and Abiotic Variables (Sánchez et al. 1985, Vaughan et al. 1996). In this sense, Mean physicochemical values of the three plots varied very the assemblages of macroinvertebrates that live in the Palo little from each other except for dissolved oxygen. However, Verde wetland are adapted to this hydroperiod as well as we found significant differences among these variables concurrent changes in temperature and salinity. Eggs are across sampling dates. This annual variation is mainly due laid and larvae begin to grow when the marsh begins to to the seasonality of the marsh (Trama et al. 2009b, Pucci fill with rainwater (Ward 1992). Generally, macroinverte- 2012), which defines the water level and consequently the brate assemblages are known to differ seasonally among physicochemical conditions. Depth is also directly related treatment areas because these taxa colonize the wetlands to the entrance of light and water temperature (Margalef at different times of the year and in different vegetation 1983, Jiménez and Springer 1996). covers (De Szalay and Resh, 2000). Management had strong effect on the structure and com- There are two possible reasons for the disproportionate position of macroinvertebrate assemblages. However, other increase of the mentioned groups in Plot B. First, it may temporal or physiochemical variables were also found to be caused by the sharp increase in the concentration of influence macroinvertebrates such as the sampling date, dissolved oxygen from January to March in plot B, when water depth, and dissolved oxygen levels. Hydroperiod it was essentially a pool of water without any vegetation. modulates the establishment of fauna and flora, and the After T. domingensis decomposes at the end of the dry cycle of rain and drought that varies throughout the year season, there is not enough time for other species of aquatic is what establishes the cycle of productivity (Roldán 1988, vegetation to grow before the water disappears completely. Vaughan et al. 1996). Likewise, the distribution of macro- Without the protection of plants, the strong winds of the invertebrates is determined by the tolerance range of each dry season likely increased the dissolved oxygen. Also, taxon to physicochemical conditions at each site (Merritt the lack of vegetation that would have been under decom- and Cummins 1996b). position may have helped conserve oxygen. Second, the Water depth is one variable that regulates the amount of macroinvertebrate groups that dominated Plot B are those solar radiation that penetrates a body of water that will be known to do well in stressful conditions. Chironomids used by aquatic plants and algae to provide chemical energy are often the most abundant (Category IV) in a variety of to other organisms (Roldán 1992). Also, solar radiation aquatic environments (McCafferty 1983, Pennack 1989, affects temperature cycles and along with rain and drought Ward 1992, Thorp and Covich 2001). The dominance of cycles, conditions the establishment of some groups of Conchostracans, gastropods, and Chironominae can be macroinvertebrates. Specifically, dissolved oxygen is one of explained by the seasonal conditions of the Palo Verde wet- the most important factors for macroinvertebrate assem- land. Conchostracans were the most abundant (Category blies, especially insects. Oxygen solubility is regulated by IV) macroinvertebrates collected during the period while temperature, so at higher temperatures the concentration the marsh is being filled (July 2004 and January–March of dissolved oxygen decreases (Roldán 1992).

186 • June 2017 ECOLOGICAL RESTORATION 35:2 Taxa richness was linearly related to both sampling aquatic macroinvertebrates inside of cover that is not easily date and water depth, increasing steadily throughout the accessible to waterfowl that do not penetrate dense veg- year, with ascending values from plot A to C. In contrast, etation (Trama 2005). Management practices that reduce abundance did not demonstrate a clear linear relationship T. domingensis and increase the amount of edge of these with either sampling date or treatment, likely due to the stands will improve the structural diversity and local outstanding abundance measured in Plot B in January habitat diversity in terms of richness and abundance of and February. High abundance values in plot B coincided macroinvertebrates at the Palo Verde wetland. However, with increased levels of dissolved oxygen. In all models, it is important to note that the findings in this study are water depth was an important factor, predicting higher specific to this wetland, and have not been extrapolated abundance and richness in open water. or replicated in other wetlands that may require similar management strategies. Recommendations for T. domingensis Management Acknowledgements The main objective of T. domingensis management was The authors thank the Organization for Tropical Studies for to create bodies of water or other vegetative coverage as funding this study and facilitating the provision of the research habitat for resident and migratory waterfowl. However, and collection permit (No. 30856). We also thank the staff of after years of T. domingensis invasion, some species of the Ministry of Environment and Energy for allowing this work. wildlife have apparently adapted to these new conditions, Thanks to Miguel Archangelsky, Luis Guillermo Chaverri Sán- including birds, mammals, amphibians and reptiles that chez, Carlos Esquivel, Katherine Quiroz, and Zaidett Barrientos use T. domingensis coverage in both rainy and dry sea- for their valuable and generous contributions in identifying macroinvertebrates. sons. Also, at least 17 species of plants have grown within T. domingensis stands (Trama et al. 2009a, Trama et al. 2009b). The removal of T. domingensis in some areas of References the wetland also increases diversity of macroinvertebrates, Ausden, M., W.J. Sutherland and R. James. 2001. The effects of flood- because some Hemiptera taxa were found only in open ing lowland wet grassland on soil macroinvertebrate prey of areas with other emerging and floating aquatic plants. breeding wading birds. Journal of Applied Ecology 38: 320–338. Some macroinvertebrate taxa appear to have adapted to Bambaradeniya, C.N.B. 2000. Ecology and biodiversity in an irrigated rice field ecosystem in Sri Lanka. PhD dissertation, T. domingensis conditions as evidenced by a greater number University of Peradeniya. of taxa and higher abundance of some taxa in the control Bambaradeniya, C.N.B. and F.P. Amarasinghe. 2003. Biodiversity plot. However, although macroinvertebrate richness was Associated with the Rice Field Agro-Ecosystem in Asian Coun- higher in areas with T. domingensis, most migratory and tries: A Brief Review. Working Paper 63. Colombo, Sri Lanka: resident birds avoid this dense vegetation cover (Trama et International Water Management Institute. al. in prep, Kostecke et al. 2005). Abundance was higher for Boza, M.A. 1981. Aves sobresalientes de Palo Verde. Biocenosis other taxa in the managed plot B, especially Chironomi- 3:23–25. Boza, M.A. and R. Mendoza. 1981. The National Parks of Costa Rica. dae, which as a group is an essential food source for some Madrid, Spain: INCAFO. wetland birds. It is said that 5000 Chironomid individuals Brown, S.C. and D.P. Batzer. 2001. Birds, plants, and macroinverte- per square meter are needed to support large numbers of brates as indicators of restoration success in new york marshes. migratory birds (Kostecke et al. 2005, Murkin and Kadlec Pages 237–248 in R.B. Rader, D.P. Batzer and S.A. Wissinger 1986). In our study, the density of chironomids was more (eds), Bioassessment and Management of North American Fresh- than 2 times higher in Plot B than in Plots A or C, which water Wetlands. New York, NY: John Wiley and Sons. suggests that Plot B could support more aquatic birds than Bufford, J.L. and E. González. 2012 Manejo del humedal Palo Verde y de las comunidades de aves asociadas a sus diferentes hábitats. the other two treatments. Ambientales 43:7–16. Macroinvertebrates are a very important source of food Calvo, J.C.A. and O.R. Arias. 2003. Avances en el monitoreo y la for waterfowl (Ausden et al. 2001, Brown and Batzer 2001, restauración hidrológica del Humedal del Parque Nacional Marklund 2002, Kostecke et al. 2005, Horppila and Nur- Palo Verde. San José, Costa Rica: Organización de Estudios minen 2001, Martin and Neely 2001). Thus, to ensure high Tropicales. macroinvertebrate biodiversity, we recommend that some Camburn, K., M. Frieze, R. Kuhn and D. Ponte. 2001. Biodiversity areas of T. domingensis remain in the marsh; stands of at impact of cattail (Typha dominguensis) dominated marsh areas least 15 m diameter would create ideal conductivity condi- in the seasonal wetlands at Palo Verde National Park. San José, Costa Rica: Environmental Sciences Institute. tions for the establishment of those macroinvertebrates that Castillo, L.E. 2000. Pesticide impact of intensive banana production develop in T. domingensis coverage. This recommendation on aquatic ecosystems in Costa Rica, PhD dissertation, Stock- coincides with that of the national park management plan holm University. to leave 10–15 m wide patches of T. domingensis (Vaughan Castillo, M. and J.A. Guzmán. 2004. Cambios en cobertura vegetal et al. 1996). These stands will favor the development of en Palo Verde según SIG. Ambientico 129:4–6.

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