Ribeiro et al. Helgol Mar Res (2019) 73:6 https://doi.org/10.1186/s10152-019-0527-9 Helgoland Marine Research ORIGINAL ARTICLE Open Access Evaluating the potential impact of bird predation on the SW Atlantic fddler crab Leptuca uruguayensis Pablo D. Ribeiro1,2* , Diego D. Navarro1, Luciano M. Jaureguy3, Pedro Daleo1 and Oscar O. Iribarne1 Abstract The southernmost permanent population of the fddler crab Leptuca uruguayensis occurs along the Samborombón Bay (36°22′S, 56°45′W, Argentina), an important feeding site for many bird species, including ruddy turnstones (Are- naria interpres), whimbrels (Numenius phaeopus), grey plovers (Pluvialis squatarola), american golden plovers (Pluvialis dominica) and gull-billed terns (Gelochelidon nilotica). Although all these birds are known to prey on many fddler crab species worldwide, there is no estimation of their joint predation impacts, probably due to the difculty in conduct- ing experiments on an appropriate spatial scale. In these situations, computer simulation methods are useful tools. By using Monte Carlo methods and feld data, we modeled the decrease of a fddler crab population due to bird preda- tion. The model found that under current bird occurrences and crab densities, birds do not consume more than 0.03% of the studied fddler crab populations. Birds only consume more than 10% of the population if crab density is below 0.02 crabs m2, or if bird occurrences are at least 3 orders of magnitude higher than currently observed. Both situations are unlikely, as mean crab density is 140 crabs m2, and bird density is never so high. Furthermore, by monitoring three diferent fddler crab patches, we found that bird predation cannot account for temporal density changes, suggesting that other population processes are more important than bird predation. In conclusion, even though fddler crabs may exhibit strong predator-avoidance behavior, direct lethal efects of bird predation are currently small. Keywords: Fiddler crabs, Uca uruguayensis, Leptuca uruguayensis, Predation impact, Shorebird predation, Computer simulation Background contradictory conclusions [11]. Predators have negli- Soft-bottom environments such as mudfats and marshes gible efects in some areas (see [12, 13]) while they sig- are important sites for biological conservation, largely nifcantly decrease prey abundances in others [7, 14], because they are feeding areas for both local and migra- and/or modify their size frequency structure [3, 15, 16]. tory bird species [1]. Indeed, most migratory shorebird Terefore, it seems that in soft bottom intertidal habi- species obtain most of their prey from these environ- tats there are conditions or sites where predation may ments (e.g. [2]), and these habitats are thus subjected to act as a strong selective force while in others it is negli- annual events of episodic predation [3] due to high densi- gible [11, 17]. Given logistic constraints, experiments ties of shorebirds stopping along their migratory path to designed to measure the impact of predation are gener- rest and feed [4–9]. ally performed on a much smaller spatial scale than the Investigations on the role of predators in soft-bottom study system [18], providing results that may deviate communities (reviewed in [10]) have often reached considerably when extrapolated to the scale of the natural system [19–21]. Extrapolation of predation impacts from low spatial scale experiments to the system scale should *Correspondence: [email protected] therefore be used with caution [21–24]. Another way of 1 Instituto de Investigaciones Marinas y Costeras (IIMyC), Facultad de Ciencias Exactas y Naturales, UNMdP-CONICET, Mar del Plata, Argentina inferring the impact of predation is through the use of Full list of author information is available at the end of the article computer model simulations (e.g. [18]). Even when they © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Ribeiro et al. Helgol Mar Res (2019) 73:6 Page 2 of 12 do not always incorporate experimental data (i.e. preda- 1.4 m) semidiurnal tides. Fiddler crabs settle forming tor exclusion experiments), computer simulations are still extensive patches with densities of up to 140 crabs m−2 powerful tools because they can easily incorporate obser- [36]. Data were obtained from an area along a 1000-m vational feld data into models on the scale of the system. long 100-m wide intertidal beach, within which we × 2 For example, computer simulations based on feld obser- identifed six fddler crab patches (mean = 1175.5 m ) vations of predator and prey behaviors may be used to separated by interpatch clear areas without settlements model the predator prey-interaction during a given time (52.98% of the observation area). Te edge of each fddler frame and on the scale of prey patches. crab patch was demarcated with 1 m wooden sticks. We Te fddler crab Leptuca uruguayensis (previously Uca considered fddler crab patches as population units and uruguayensis) is a small (up to 16.5 mm carapace width; explored their population size changes due to bird preda- see [25]) intertidal species found from southern Brazil tion using Monte Carlo methods [37]. (33°S) to the northern coast of Argentina (38°S; [25, 26]). Te southernmost permanent population occurs along Bird and fddler crab data the Samborombón Bay (36°22′S, 56°45′W, Argentina; see In the study area, the fddler crab Leptuca uruguayensis is [27]), where it is found mainly on exposed wet mudfats commonly preyed upon by ruddy turnstones, whimbrels, from the middle to upper intertidal fats near the fringe grey plovers, american golden plovers and gull-billed of an extensive Sporobolus densiforus (previously Spar- terns (see [31]). Te model used the data from crab and tina densifora) marsh. Tis area is an important stopover bird surveys and observations performed during difer- site for many non-tropical birds [28–30], where fddler ent feld trips (3 to 5 days each), during 1999, 2000 and crabs provide food for several species, including ruddy 2001. On each trip, we measured the size of each of the turnstones (Arenaria interpres), whimbrels (Numenius six fddler crab patches. Each day, surveys of birds in each phaeopus), grey plovers (Pluvialis squatarola), american of the identifed fddler crab patches were carried out on golden plovers (Pluvialis dominica) and gull-billed terns an hourly basis, beginning 5 h before the diurnal low tide (Gelochelidon nilotica; see [31]). In some areas, fddler and ending 5 h after it, encompassing the time frame dur- crabs may be the main food source for several bird spe- ing which the mudfats were exposed. In addition, hourly cies (e.g. [32, 33]), suggesting that predation impact on surveys of fddler crab activity were carried out by taking fddler crabs should be considerable. In addition, each 5 samples (in each fddler crab patch) and counting the bird species has diferent feeding tactics and rates, lead- number of male and female crabs within a 5 m × 1.5 m ing to the consumption of diferent proportions of female focal area. Focal observations over 207 individual birds, and male crabs [31, 34, 35]. Te global efect of predation totaling 884 min of audio-tape recordings provided data on crab population size and sex ratio would therefore to compute their feeding rates. During each observation, depend on both the number and relative occurrence of the observer continuously reported all behaviors of the each bird species. focal individual, including prey capture attempts and out- In this context, we constructed a mathematical model comes, and prey items captured. Male fddler crabs were and applied Monte Carlo computer simulations to evalu- easily identifed from females when captured by the red ate the potential predation impact of birds on a South- color of their enlarged claw. Data on bird occurrences, western Atlantic fddler crab population of the species feeding rates and the used methodology have been par- Leptuca uruguayensis. Using bird and fddler crab feld tially published [34, 35, 38]. observations, we (1) evaluated the potential impact of Fiddler crabs dig burrows that are used for mating, egg predation under diferent fddler crab population den- incubation by females, and as temporary refuges from sities and under natural bird occurrences, (2) evaluated predators and physiological stress (e.g. high or low tem- how predation impact would change if bird occurrences peratures, high tides). For the study site (a temperate were higher than currently observed in nature and, (3) zone) fddler crabs show a succession of surface activ- compared the density changes due to bird predation ity over a year, from mid-September up to mid-March, expected by the model to the population density changes represented by 3 diferent periods: (1) feeding only, (2) of three fddler crab patches monitored in the feld. reproduction and feeding, and (3) feeding only. Tus, with the arrival of spring, fddler crabs resume sur- Methods face activity, feeding and growing exclusively for about Study site 2 months; after which they initiate the reproductive Te study used a database obtained from feld observa- period, which may last 2–3 months, and fnally return tions at intertidal mudfats near the mouth of San Cle- to feeding only for about 2 months before completely mente tidal creek (eastern Samborombón Bay, 36°22′S, halting surface activities when winter begins. Tis time 56°45′W, Argentina), an area with low-amplitude (up to frame coincides with the presence of migratory bird Ribeiro et al. Helgol Mar Res (2019) 73:6 Page 3 of 12 species that use fddler crabs as a prey item [30, 31].