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Macrophytes As Refuge Or Risky Area for Zooplankton: a Balance Set by Littoral Predacious Macroinvertebrates

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Macrophytes As Refuge Or Risky Area for Zooplankton: a Balance Set by Littoral Predacious Macroinvertebrates Freshwater Biology (2009) 54, 1042–1053 doi:10.1111/j.1365-2427.2008.02152.x Macrophytes as refuge or risky area for zooplankton: a balance set by littoral predacious macroinvertebrates ,1 †, 1 GONZA´ LEZ SAGRARIO*, MARI´A DE LOS A´ NGELES* , ESTEBAN BALSEIRO ,ROMINA ITUARTE*,1 AND EDUARDO SPIVAK*,1 *Departamento de Biologı´a, Universidad Nacional de Mar del Plata, FCEyN, Mar del Plata, Argentina †INOBIOMA, CONICET – Universidad Nacional del Comahue, Centro Regional Universitario Bariloche, San Carlos de Bariloche, Argentina 1CONICET (Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas). SUMMARY 1. Zooplankton use macrophytes as day-time refuge areas when trying to escape from pelagic predators. But macrophytes can also host a diverse and abundant macroinverte- brate assemblage and zooplankton are also likely to face predacious macroinvertebrates once they enter the littoral zone. This study aimed to elucidate the role of macro- invertebrates in determining the refuge capacity of macrophytes. 2. We conducted a field enclosure experiment using plastic bags and complementary laboratory feeding trials to test how macroinvertebrates counteract the benefits to zooplankton of the macrophyte refuge. The field experiment consisted of three treatments with different macroinvertebrate assemblages: without predators (WP), low abundance and diversity (LAD) and high abundance and diversity of predators (HAD – which represents lake conditions). 3. Populations of Diaphanosoma brachyurum, Bosmina huaronensis and Moina micrura (Cladocera) and of both male and female Notodiaptomus incompositus (Copepoda, Calanoida) declined (by nearly 80%) in the presence of HAD in comparison to WP and LAD treatments. 4. Feeding trials revealed that Buenoa sp. (backswimmer), adults of Palaemonetes argentinus (grass shrimp) and Cyanallagma interruptum (damselfly) had a significant negative impact on cladocerans (D. brachyurum, B. huaronensis) and the calanoid copepod population (males, females and copepodites). These predators showed a strong predation effect ranging from 75% to 100% reductions of zooplankton populations. 5. The refuge effect offered by macrophytes to zooplankton depends on and is balanced by the predacious macroinvertebrate assemblage that plants host. The risk of confronting littoral predators is high and macroinvertebrate presence can turn the macrophytes into risky areas for zooplankton. Keywords: macroinvertebrates, macrophytes, predation, refuge, zooplankton is correlated with a clear water phase (Timms & Moss, Introduction 1984; van den Berg et al., 1998), promoted by mech- Macrophytes are key organisms in shallow lakes as anisms including reductions in sediment resuspen- they modify trophic interactions and other aspects of sion, wave and wind action (Barko & James, 1998; lake functioning. Their establishment and dominance Horppila & Nurminen, 2003), and the provision of Correspondence: Gonza´lez Sagrario, MA, Departamento de Biologı´a, Universidad Nacional de Mar del Plata, FCEyN, CC 1245, (7600) Mar del Plata, Buenos Aires, Argentina. E-mail: [email protected] or [email protected] 1042 Ó 2008 The Authors, Journal compilation Ó 2008 Blackwell Publishing Ltd Macroinvertebrate predation in macrophyte stands 1043 refuges for zooplankton that promote higher grazing whether predacious invertebrates counteract the ref- rates on phytoplankton (Schriver et al., 1995; Sønderg- uge offered by macrophytes. aard & Moss, 1998; Scheffer, 1999). Several studies have reported the migration of zooplankton to the edge of macrophyte stands during Methods daytime (diel horizontal migration, DHM) to seek Study site refuge from planktivorous fish (Schriver et al., 1995; Lauridsen & Buenk, 1996; Lauridsen et al., 1998). Los Padres Lake, located in Buenos Aires Province of Large zooplankton species, like Daphnia, and even Argentina (Pampa Plain, at 37°55¢ and 38°02¢S and smaller ones, like Ceriodaphnia, display horizontal 57°34¢ and 57°33¢W) is a small, shallow, eutrophic lake migrations (Lauridsen & Buenk, 1996; Stansfield et al., (area = 2 km2; mean depth = 1.8 m) with a polymictic 1997; Moss, Kornijo´w & Measy, 1998). The effective- thermal regime and alkaline water (pH = 8.6). The ness of macrophytes as refuge areas depends on transparency is variable with turbid and clear periods various factors including plant architecture, size, varying from year to year (Secchi disk depth ranged shape and density of plant patches, and also on the from 40 to 90 cm during 1998–2002). Values for ) predators that these plants host (Jeppesen et al., 1998). chlorophyll-a ranged from 20 to 90 lgL 1 and for ) Indeed, macrophytes provide habitat for predacious total phosphorus from 100 up to 400 lgL 1 during macroinvertebrates, including odonates, notonectids, 1999–2001 (M. Gonza´lez Sagrario, unpubl. data). dytiscid beetles and water mites, which could exert a In the littoral zone of Los Padres Lake, the bulrush strong predation impact on zooplankton populations Schoenoplectus californicus (Meyer) Steud. constitutes (Balseiro, 1992; Hirvonen, 1999; Hampton, Gilbert & an outer ring around the whole lake, while in the Burns, 2000). In shallow lakes, therefore, zooplankton inner part and near emergent plants, different species must face planktivorous fish and predacious inverte- of submerged macrophytes dominate, such as Pota- brates in the pelagic zone, and benthic, epiphytic and mogeton pectinatus Ruiz and Pavo´n and Ceratophyllum epineustonic invertebrate predators in the littoral demersum L. Plant coverage varies inter-annually, and zone. As a consequence, the benefit of escaping from in some years submerged plants are absent. Vegetated pelagic predators must be balanced with the cost of areas host small- to medium-sized fish species, birds confronting predators in the littoral zone. and a rich macroinvertebrate assemblage. Direct predation on zooplankton by epiphytic and In open waters, the zooplankton community is benthic invertebrates is a potentially large, and over- mainly composed of small- to medium-sized cladoc- looked, cost of DHM (Burks et al., 2002). Most studies erans including Bosmina (Neobosmina) huaronensis De- supporting the effectiveness of DHM as an anti- lachaux, Ceriodaphnia dubia Richard, Moina micrura predator behaviour have focused on northern tem- Kurz, and Diaphanosoma brachyurum (Lievin). Sporad- perate lakes (Burks et al., 2002), mainly in Europe. In ically the large cladoceran species Daphnia (Cteno- contrast, knowledge about the effectiveness of macro- daphnia) spinulata Birabe´n also occurs. Two species of phytes as refuge areas for zooplankton from tropical calanoid copepods are present – Notodiaptomus incom- and subtropical as well as temperate areas from the positus (Brian) and Boeckella bergi Richard, with southern hemisphere is limited (Burks et al., 2002; N. incompositus being the dominant species. Acantho- Gonza´lez Sagrario, 2004). Moreover, the lack of a cyclops robustus (Sars) dominates the cyclopoid cope- DHM pattern for cladoceran species has been associ- pod assemblage (Gonza´lez Sagrario, 2004). ated with the presence of predacious macroinverte- In littoral areas, macrophytes host a very rich and brates in the littoral zone of some New Zealand and diverse macroinvertebrate assemblage, comprised the North America lakes (Smiley & Tessier, 1998; Laurid- predacious odonates [Coenagrionidae – Cyanallagma sen et al., 1999). Still, the role of macroinvertebrates interruptum (Selys) and C. bonariense (Ris)- and Aes- and how they can alter macrophyte refuge provision hnidae – Aeshna sp.], hemipterans [Notonecta sp. and are not well understood or documented. Our objective Belostoma elegans (Mayr)], hydrophillid larvae (Berosus in this study is to assess the cost associated with the sp.), flatworms (Mesostoma ehrenbergii Focke), water use of macrophyte stands when these host a rich mites (mainly Unionicolidae, Koenikea curvipes Rosso assemblage of macroinvertebrates and to determine de Ferrada´s, and also Arrenurus oxyurus Rosso de Ó 2008 The Authors, Journal compilation Ó 2008 Blackwell Publishing Ltd, Freshwater Biology, 54, 1042–1053 1044 G. Sagrario et al. Ferrada´s, Eylais multiespina Ribaga, Hydrachna sp. and whole water column with a Schindler-Patalas trap Limnesia sp.) and the grass shrimp Palaemonetes (6 L) and storing it in two buckets. Then, after mixing argentinus (Nobili) (Gonza´lez Sagrario, 2004). Macro- the water 10 times in each bucket, we took 1 L with a invertebrates show a strong association with macro- graduated beaker to fill each enclosure. After pouring phyte stands, occupying the inner parts and ⁄or edges 1 L into each bag, the remaining water in the buckets of vegetated patches during day and night, with was discharged and fresh water was collected. This potential zooplankton predators reaching very high procedure lasted until each enclosure had a final abundances (e.g. sum of C. bonariense and C. interrup- volume of 13 L. This methodology followed that of ) ) tum: 150–200 ind. m 2, P. argentinus: 20–30 ind. m 2) Hampton et al. (2000) to achieve a homogeneous (Gonza´lez Sagrario, 2004). zooplankton distribution amongst replicates and a representative zooplankton in terms of abundance and assemblage. Experiment 1: Effect of littoral macroinvertebrate Macroinvertebrate collection occurred in Las Nu- diversity and abundance on zooplankton populations trias Lake (close to our lake), because in Los Padres We performed a field enclosure experiment in the Lake no macrophyte stands appeared in summer 2003
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