Wetlands (2015) 35:723–732 DOI 10.1007/s13157-015-0664-0 ORIGINAL RESEARCH Fallen Nestlings and Regurgitant as Mechanisms of Nutrient Transfer from Nesting Wading Birds to Crocodilians Lucas A. Nell1 & Peter C. Frederick1 Received: 18 February 2015 /Accepted: 13 May 2015 /Published online: 6 June 2015 # Society of Wetland Scientists 2015 Abstract Positive interspecific interactions can shape funda- Keywords Alligator mississippiensis . Facilitation . Food mental wetland ecosystem dynamics, including energy trans- subsidy . Nest protection . Everglades fer and spatial distribution of nutrients. Birds, by foraging in one location and nesting in another, commonly act as between-ecosystem nutrient vectors. However, the distribu- Introduction tion of nutrients within nesting areas and mechanisms of trans- fer to other trophic levels are poorly understood. We report on Positive ecological interactions have received much attention measurements of available food transferred from nesting long- as structuring mechanisms shaping populations and commu- legged wading birds to American alligators (Alligator nities (Bertness and Callaway 1994;Stachowicz2001; Bruno mississippiensis) in the Everglades of Florida, USA. Using et al. 2003; Kiers et al. 2010). One common currency of pos- throughfall traps, a historic dataset on nesting success and a itive exchange is the transfer of nutrients (Stachowicz 2001). literature-parameterized alligator energy budget, we estimated When species’ demographic or life history strategies employ the potential food available to alligators via regurgitant and movement across habitat boundaries, these organisms can cre- nestling carcasses, and compared that to alligator food require- ate strong nutrient links between ecosystems and enrich nutri- ments. Although dropped regurgitant is of little importance to ent regimes for entire communities. Pacific salmon scavenging alligators, we estimate that nestling carcasses (Oncorhynchus spp.), for instance, fertilize the freshwater riv- throughout the ecosystem could support the energetic require- ers in which they spawn with marine-derived nutrients they ments of hundreds of alligators for periods of several months. accumulate while feeding at sea. These subsidies can pass This resource occurs during the dry season, when alligator through additional nutrient transport vectors to affect aquatic, thermoregulatory opportunities are relatively scarce and fe- riparian and terrestrial communities, from primary producers male alligators are mobilizing resources for egg-laying. Our to apex predators (Hilderbrand et al. 1999;Helfieldand results indicate that through fallen nestlings, wading bird Naiman 2001; Chaloner et al. 2007;Janetskietal.2009; nesting colonies have strong potential to benefit alligators. Hocking and Reynolds 2011). This facilitative exchange may be globally widespread, Nutrient transfer underlies many fundamental wetland eco- forming a keystone process in many tropical and subtropical system processes as well (Bertness 1984; Frederick and wetlands. Powell 1994; Ellison et al. 1996; Høberg et al. 2002), and large populations of birds that breed colonially in wetlands frequently act as significant nutrient vectors (Bildstein et al. 1992; Frederick and Powell 1994). Nesting waterbirds can consume large amounts of prey over a nesting season: a col- * Lucas A. Nell ony of 500 wood stork (Mycteria americana) pairs, for exam- [email protected] ple, is estimated to consume over 100,000 kg of fish during a breeding season (Kahl 1964). A portion of those nutrients are 1 Department of Wildlife Ecology and Conservation, University of inevitably concentrated near nesting colonies. In the Florida, P.O. Box 110430, Gainesville, FL 32611, USA Everglades, typical nesting colonies of long-legged wading 724 Wetlands (2015) 35:723–732 birds (herons, egrets, ibises, storks, and spoonbills; simply above American alligators (Alligator mississippiensis), and Bwading birds^ hereafter) are estimated to deposit phosphorus that there is a mutually exclusive distribution of alligators at about 20 times the areal atmospheric deposition rates and mammalian predators (Burtner 2011). Together with evi- (Frederick and Powell 1994), and a white ibis (Eudocimus dence that alligators readily target and consume mammals albus) colony in Okefenokee Swamp, Georgia showed vege- (Shoop and Ruckdeschel 1990;Barr1997;Rice2004), there tative effects of nutrient enrichment years after it was aban- is reasonably strong evidence that alligators deter mammalian doned by birds (Oliver and Schoenberg 1989). nest predators. It remains unclear whether alligators also ben- The fate and mechanisms of transfer of such large quanti- efit from associating with wading bird colonies. ties of deposited nutrients in breeding colonies are not well We hypothesize that alligators benefit from associating understood. Although one obvious mechanism is bottom-up with wading bird nesting colonies via one or a combination food web effects through nutrient enrichment of waters and of the following mechanisms: (1) fallen material from nests soil, there may also be more direct transfer to predators and (e.g., nestlings, regurgitant), (2) predation on adult and juve- scavengers. Crocodilians are top predators and scavengers in nile birds, (3) greater nearby aquatic prey abundance fueled by many subtropical and tropical wetlands, and have diverse diets nutrients in bird guano, and (4) consumption of nest predators (McIlhenny 1935; Taylor 1979; Delany and Abercrombie drawn to colonies. We report here on measurement of the 1986; Wolfe et al. 1987; Magnusson et al. 1987;Barr1997; potential energy available to alligators from nestling carcasses Gabrey 2010; Rosenblatt et al. 2015). Crocodilians have been and dropped regurgitant in wading bird colonies, and use a observed routinely eating chicks that fall out of nests into the modeled alligator energy budget to assess the significance of water in breeding colonies (Dusi and Dusi 1968; Coulter and energy derived from colonies. We predict that the food poten- Bryan 1995), and large regurgitant meals may also be acci- tially available from wading bird colonies is non-trivial to dentally dropped or purposefully vomited by adult birds and alligators and that most of these benefits are in the form of chicks (Byers 1951; Furness and Hislop 1981; Coulter et al. nestling carcasses. 1999; Clarke and Prince 2008; Nell 2014). Many colonial nesting birds lay more eggs than they can raise and adjust brood size to fit available food resources through several pro- Methods cesses of brood reduction (Ricklefs 1965;O’Connor 1978; Clark and Wilson 1981;Mock1984, 1985;Stenning1996). Study Area This often amounts to 1–2 chicks being ejected alive or dead from each nest, and this may be an important form of nutrient The study area encompassed Water Conservation Areas 1–3 deposition that comes in an appropriate package for large- (WCAs) of the Everglades, a ~3500 km2 wetland region in bodied carnivores like crocodilians. Miami-Dade, Palm Beach, and Broward Counties, Florida Some birds may seek out breeding locations near crocodil- (Fig. 1). The field research took place in Water Conservation ians. Several papers describe birds consistently nesting over Areas 3A (WCA 3A) and 3B (WCA 3B). Most of WCA 3A water with crocodilians present (Dusi and Dusi 1968;Jenni consists of ridge-and-slough landscape: slightly elevated 1969; Robinson 1985;PostandSeals1991, 1993; Coulter and ridges dominated by sawgrass (Cladium jamaicense)withem- Bryan 1995). Hudgens (1997) even demonstrated that blue- bedded tree islands of coastalplain willows (Salix billed malimbes (Mulimbus nitens) positioned their nests in caroliniana), swamp bay (Persea palustris), dahoon holly clusters around African dwarf crocodile (Osteolaemus (Ilex cassine), and other trees/shrubs, and deeper-water tetraspis) dens along flooded river banks in Ghana. This ap- sloughs dominated by floating aquatic plants (e.g., parent attraction may be to utilize crocodilian presence for Nymphaea odorata, Utricularia spp.). WCA 3B comprises protection from nest predators: crocodilians are largely unable sparse sawgrass (C. jamaicense) marsh dotted by small to access nests by climbing (but see Dinets et al. 2014), but willow-dominated tree islands, and pond apple trees themselves consume many ground-based nest predators (Annona glabra) that line partially filled-in canals (for more (Taylor 1979;Magnussonetal.1987; Shoop and detail, see Lodge 2010). Wading bird nesting colonies are Ruckdeschel 1990; Barr 1997; Luiselli et al. 1999). predominantly located in inundated, lower-elevation islands For the large, mixed-species, wading bird nesting colonies with the longest hydroperiods; in our study area these islands in the southeastern United States, medium-sized, semiaquatic are typically dominated by willow (Frederick and Collopy mammals such as raccoons (Procyon lotor) and opossums 1989a). (Didelphis virginiana) present the greatest nest predation threat. Even small numbers of these nocturnal predators can Dropped Regurgitant cause entire wading bird colonies to abandon their nests (Rodgers 1987; Frederick and Collopy 1989a). Recent re- To quantify fallen regurgitant from nests, we placed search suggests that wading birds actively choose nesting sites throughfall traps in two nesting colonies in 2013– Wetlands (2015) 35:723–732 725 Alabama Georgia marked for nest success observations and throughfall trap placement. We placed traps at random distances (0–5m)and Atlantic