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Density and Traitmediated Topdown Effects Modify Oikos 122: 790–800, 2013 doi: 10.1111/j.1600-0706.2012.20696.x © 2012 The Authors. Oikos © 2012 Nordic Society Oikos Subject Editor: Jotaro Urabe. Accepted 28 June 2012 Density- and trait-mediated top–down effects modify bottom–up control of a highly endemic tropical aquatic food web C. M. Dalton, A. Mokiao-Lee, T. S. Sakihara, M. G. Weber, C. A. Roco, Z. Han, B. Dudley, R. A. MacKenzie and N. G. Hairston Jr. C. M. Dalton ([email protected]), M. G. Weber, Z. Han and N. G. Hairston Jr., Dept of Ecology and Evolutionary Biology, Cornell Univ., Ithaca, NY 14853, USA. – A. Mokiao-Lee and T. S. Sakihara, Tropical Conservation Biology and Environmental Science Graduate Program, Univ. of Hawai‘i at Hilo, Hilo, HI 96720, USA. TSS also at: Dept of Land and Natural Resources, Division of Aquatic Resources, 75 Aupuni St., Room 204, Hilo, HI, 96720, USA. – C. A. Roco, Dept of Microbiology, Cornell Univ., Ithaca, NY 14853, USA. – B. Dudley, Dept of Biology, Univ. of Hawai‘i at Hilo, Hilo, HI 96720, USA. – R. A. MacKenzie, USDA, Forest Service Pacific Southwest Research Station, Inst. of Pacific Islands Forestry, 60 Nowelo Street, Hilo, HI 96720, USA. Benthic invertebrates mediate bottom–up and top–down influences in aquatic food webs, and changes in the abundance or traits of invertebrates can alter the strength of top–down effects. Studies assessing the role of invertebrate abun- dance and behavior as controls on food web structure are rare at the whole ecosystem scale. Here we use a comparative approach to investigate bottom–up and top–down influences on whole anchialine pond ecosystems in coastal Hawai‘i. In these ponds, a single species of endemic atyid shrimp (Halocaridina rubra) is believed to structure epilithon communities. Many Hawaiian anchialine ponds and their endemic fauna, however, have been greatly altered by bottom–up (increased nutrient enrichment) and top–down (introduced fish predators) disturbances from human devel- opment. We present the results of a survey of dissolved nutrient concentrations, epilithon biomass and composition, and H. rubra abundance and behavior in anchialine ponds with and without invasive predatory fish along a nutrient con- centration gradient on the North Kona coast of Hawai‘i. We use linear models to assess 1) the effects of nutrient loading and fish introductions on pond food web structure and 2) the role of shrimp density and behavior in effecting that change. We find evidence for bottom–up food web control, in that nutrients were associated with increased epilithon biomass, autotrophy and nutrient content as well as increased abundance and size of H. rubra. We also find evidence for top–down control, as ponds with invasive predatory fish had higher epilithon biomass, productivity, and nutri- ent content. Top–down effects were transmitted by both altered H. rubra abundance, which changed the biomass of epilithon, and H. rubra behavior, which changed the composition of the epilithon. Our study extends experimental findings on bottom–up and top–down control to the whole ecosystem scale and finds evidence for qualitatively different effects of trait- and density-mediated change in top–down influences. Benthic invertebrates are important mediators of top– (Zaret and Suffern 1976, Mittelbach 1981, Parkos and down and bottom–up influences in many aquatic food Wahl 2010). Such trait-driven change in top–down con- webs (Wallace and Webster 1996). Increased productivity trol may be especially important in isolated ecosystems, at the base of the food web can increase benthic inverte- where behavioral or biomass compensation by other brate abundance (Gruner 2004, Slavik et al. 2004, Cross members of the community may be constrained by a et al. 2006), whereas predators can reduce invertebrate lack of diversity (Loreau et al. 2002, Duffy 2002, Covich abundance through consumption (Obernborfer et al. 1984, et al. 2004). Gilliam et al. 1989). Herbivorous invertebrates also act Despite the potential importance of trait-mediated top– as agents of top–down control, as their feeding alters the down control, its strength has rarely been assessed at abundance, diversity and productivity of photosynthetic the whole ecosystem scale, especially relative to density- organisms (Rosemond and Mulholland 1993, Hillebrand mediated or bottom–up influences. Most of the few whole- and Kahlert 2001). The strength of this top–down effect ecosystem studies contrasting top–down and bottom–up is itself sensitive to both top–down and bottom–up change control do not attempt to partition trait- from density- in food webs: increased resource abundance decreases mediated effects (Carpenter et al. 1996, Jeppesen et al. the foraging rate of invertebrates (Anholt and Werner 2000, 2003, Norlin et al. 2005, Hambright et al. 2007, 1995, 1998), and predation risk reduces the foraging Hoekman 2011, Friederichs et al. 2011). Nearly all studies rate and time spent in vulnerable habitat by consumers contrasting trait and density-mediated effects of consumers, 790 moreover, rely on experimental mesocosms or microcosms whole-ecosystem responses to the long-term modification that are subject to design-specific effects, and many do of bottom–up and top–down control in highly endemic not seek to contrast top–down and bottom–up influences food webs and provide an opportunity for insight into the (Trussell et al. 2006, Werner and Peacor 2006, reviewed relative influence of trait and density-mediated top–down by Werner and Peacor 2003, Schmitz et al. 2004). effects. Expanding evidence to whole ecosystem studies that assess Here we present the results of a comparative field both trait and density-mediated top–down control rela- survey of epilithon biomass and nutrient content, as well tive to bottom–up influences is important for understand- as H. rubra abundance and behavior in 10 anchialine ing how ecosystems may respond to changes in abiotic ponds with and 10 without invasive poeciliid fish across and biotic conditions. an established nutrient concentration gradient along Hawaiian anchialine ponds are land-locked, mixo- the North Kona coast of Hawai‘i island. The goal of this haline pools that are tidally influenced by subsurface water- survey is to assess, at the whole-ecosystem scale, the rela- table links (Holthuis 1973, Brock et al. 1987) and are tive strengths of these forces in structuring food web dyna- ideal systems for assessing the long term influence of top– mics and to enable managers to account for these forces in down and bottom–up changes to low diversity food webs. making decisions that buffer anchialine ponds from human The invertebrate biomass of these ponds is dominated development. by a single endemic atyid shrimp Halocaridina rubra, the grazing of which is thought to maintain the short- turfed, diverse epilithon typical of intact anchialine ponds Methods (Bailey-Brock and Brock 1993). Deep accumulations of organic matter, however, have replaced this epilithon Site description ‘lawn’ in ponds near human development (Bailey-Brock and Brock 1993, Wiegner et al. 2006). This change may In January 2011, we surveyed 20 anchialine pools selected stem from a bottom–up effect, nutrient loading that has from among several hundred known ponds along the occurred since the construction of nearby resorts in the mid North Kona coast of Hawai‘i Island (Fig. 1, Table 1). All 1990s (Wiegner et al. 2006), or a top–down effect, the ponds were within 100–250 m of the shoreline and were introduction of predatory non-native poeciliid fish. These selected based on the presence or absence of human devel- top predators may reduce grazing pressure by reducing the opment along each pond’s immediate periphery and the numerical abundance of H. rubra through consumption presence or absence of invasive poeciliid fish. Seven of or by reducing the time H. rubra spends feeding, releasing the surveyed ponds had human development on their the epilithon from top–down control (Capps et al. 2009, immediate periphery and thirteen had no development Carey et al. 2010, MacKenzie and Bruland 2011). These within several hundred meters (often much more). The ponds thus provide a ‘natural’ experiment for the study of seven ponds near human development were located on Figure 1. Map of the North Kona Coast on the island of Hawai‘i showing the four study site locations. 791 Table 1. List of ponds surveyed and their environmental properties. 2 Habitat Surface Max Mean NO2 1 Mean Mean Mean 2 2 1 Site Pool name periphery area (m ) depth (m) NO3 (mM) NH4 (mM) DIN (mM) SRP (mM) Fish ‘Anaeho‘omalu AB12 undeveloped 36.2 0.5 50.99 1.90 52.90 1.88 ‘Anaeho‘omalu AB14 undeveloped 62.8 0.5 58.51 1.78 60.29 2.11 ‘Anaeho‘omalu AB16 undeveloped 3.4 —* 50.38 2.73 53.11 1.90 ‘Anaeho‘omalu AB17 undeveloped 2.5 — 51.03 2.00 53.03 1.90 ‘Anaeho‘omalu AB18 undeveloped 8.3 — 55.99 1.93 57.92 2.01 ‘Anaeho‘omalu AB5 undeveloped 2.9 0.6 58.27 3.40 61.68 2.15 ‘Anaeho‘omalu AB6 undeveloped 104.9 0.8 54.65 1.97 56.62 1.97 Huala–lai Waiiki developed 77.2 — 145.61 3.09 148.70 5.53 Kona Village KVBP developed 30.9 0.6 109.84 9.06 118.89 7.93 Kona Village KVPM4 developed 128.7 0.3 105.66 3.82 109.48 9.27 No fish ‘Anaeho‘omalu AB11 undeveloped 1.8 0.2 56.73 2.28 59.01 2.01 ‘Anaeho‘omalu AB13 undeveloped 9.5 — 58.27 1.97 60.24 2.13 ‘Anaeho‘omalu AB15 undeveloped 6.7 0.35 58.60 2.01 60.61 2.20 Huala–lai Ho‘onanea developed 431.2 — 125.46 3.15 128.61 7.99 Huala–lai Wai‘olu developed 282.7 — 162.43 3.98 166.41 6.91 Huala–lai Wahi Pana developed 1.1 — 181.75 2.25 183.99 6.00 Kona Village KVWB developed 1.2 0.5 77.51 6.09 83.60 7.53 ‘Akahukaimu WW10 undeveloped 8.7 — 76.59 1.52 78.10 1.72 ‘Akahukaimu WW2 undeveloped 32.8 0.6 80.10 1.51 8.61 1.59 ‘Akahukaimu WW5 undeveloped 202.8 1.25 74.52 1.62 76.14 1.79 *line indicates pond was shallower than 0.2 m.
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