The land crab Johngarthia planata (Stimpson, 1860) (Crustacea, Brachyura, Gecarcinidae) colonizes human-dominated ecosystems in the continental mainland coast of Mexico

Abstract The land crab Johngarthia planata (Stimpson, 1860) has been reported from the Baja California Peninsula and several oceanic islands in the Eastern Pacific as well as inshore islands of the Mexican, Costa Rican and Colombian coast. However, the species has not been observed on the continental mainland, as it is likely that the high diversity of terrestrial predators/competitors make the establishment of mainland populations nearly impossible. In this contribution, several new records of this species that have been observed in urban areas along the continental Pacific coast of Mexico are reported. These records demonstrate that the presence of humans does not necessarily have a negative impact on land crab species. Indeed, the presence of humans may actually discourage the presence of native crab predators/competitors and hence increase the likelihood of a successful mainland settlement of land crab species that are otherwise island and peninsula restricted. The presence of Johngarthia planata is ecologically relevant for coastal forests because gecarcinid crabs significantly influence plant recruitment and Johngarthia planata is considerably larger than the mainland species Gecarcinus quadratus.


Introduction
Macroevolutionary transitions between marine and non-marine habitats are uncommon and rarely lead to long-term success in the invaded habitat (Vermeij and Dudley 2000). This is largely due to terrestrial niches being occupied by groups with a longer evolutionary history in these habitats as well as the marine invaders' lack of traits withwhich to successfully confront the differences in terrestrial selection regimes (Vermeij and Dudley 2000).
However, while their larvae still develop in marine habitats, adults of the crab family Gecarcinidae have successfully conquered island habitats, where they play an important ecological role (Lindquist et al. (2009) for a review). Species of the Gecarcinus-group (including Johngarthia, Gecarcinus and Gecarcoidea (Türkay 1987) are dominant through sheer numbers, on some islands their mass exceeds the total mass of animals reported in tropical rain forests in Costa Rica and the central Amazon (Lindquist et al. 2009) and they may occupy the top of the energy pyramid (Burggren and McMahon 1988). Nevertheless, despite their success on islands and possible dispersal in their larval stage via sea currents, most species of the Gecarcinus-group are absent from continental mainland habitats (Türkay 1987; see Paulay and Starmer 2011). One reason for this may be the predictable mass migrations to the coast for larval release (e.g. Linnaeus 1758, Hicks 1985, Hartnoll 2011, which may render species of this group especially vulnerable to terrestrial predators, therefore limiting dispersion and the chances of success on the continental mainland. The negative impact on populations exerted by e.g. terrestrial vertebrates is supported by observed population declines or extinctions after island settlements by humans, which often actively hunt land crabs, or after the anthropogenic introduction of crab predators/competitors such as rats, feral cats and pigs (Paulay and Starmer 2011).
Johngarthia planata (Stimpson, 1860) appears to be a textbook example for the group's failure to establish itself on the continental mainland despite the advantages of ecological flexibility and favorable larval dispersion patterns (reviewed by Perger et al. 2013). Johngarthia planata occurs on the Baja California Peninsula and several oceanic islands in the Eastern Pacific as well as on inshore islands of the Mexican, Costa Rican and Colombian coasts. This wide presence is likely the result of amplified dispersal via coastal currents (Perger et al. 2013). However, likely due to the large diversity of terrestrial predators/competitors, J. planata has not been observed on continental mainland locations until now (Perger et al. 2013).
In this study I report the first continental mainland records for J. planata and discuss the possibility that human presence might actually facilitate the mainland settlement of such a species.

Materials and methods
The present study encompasses the Pacific coast from Mexico to Colombia. Following Grismer (2000) and Riddle et al. (2000) the Baja California peninsula is treated separately to the rest of Mexico, which is referred to throughout the text as "Mexican mainland" or "continental mainland" respectively. To investigate the mainland presence/absence patterns of J. planata I performed an Internet search via Google.com (search function "images") and flickr.com. Flickr is an image hosting web site that is reported to host more than 6 billion photographs. Users uploading their photos to Flickr are able to add key words ("tags") that facilitate a search on Flickr and also in web search services such as Google and Yahoo. I searched with various combinations of the key words "crab" or "cangrejo" (Spanish for crab) and "Pacific, Mexico, Guatemala, El Salvador, Nicaragua, Costa Rica, Panama, Colombia"; and all regions of the respective countries with access to the Pacific coast. I then considered for evaluation only individuals on photographs from locations that were confirmed by the photographers and demonstrated clearly visible characteristics of J. planata (see Perger et al. 2013

Analysis
The Internet search revealed photographs of 12 individuals from Mexico (mainland) and three individuals from Panama (Iguana Island) ( Table 1, Figs 1, 2). The diagnostic characters used (both apical lobes of the third maxilliped merus subequal, the leg spines prominently developed, the carapace depressed and the dark red color with orange chelipeds and cream cutting edges) (Fig. 1) were consistent with other examined specimens found on islands in Mexico and Costa Rica (Perger et al. 2013) as well as on Gorgona Island, Colombia (see Shih 2013). The specimens found on the Mexican mainland are the first continental mainland specimens ever recorded, and the specimens on Iguana Island are the first recorded in Panama. The species has been previously reported by Bright and Hogue (1972) and Jiménez et al. (1994) for "Panama" in error, likely following the reference "Malpelo Island, off Bay of Panama" by Rathbun (1918). Malpelo Island is inhabited by J. malpilensis, but the island is part of Colombia.  Island and mainland records for Johngarthia planata obtained from the literature (L) and photographs (P); new records highlighted by (*).
All mainland records of J. planata cited here refer to tourist beaches close to villages or small cities. Several photographs show individuals of J. planata foraging diurnally, running along house walls or even inside of houses and mating (Fig. 1).
The Internet search did not reveal any photographs of J. planata from Guatemala, El Salvador, Nicaragua and Costa Rica. For the latter country, the only known records to date are those cited by Perger et al. (2013). Paulay and Starmer (2011) attribute the absence of land crab species on the continental mainland to the presence of predators. However, this pattern is less pronounced in the Neotropics where Cardisoma crassum, C. guanhumi, Gecarcinus lateralis and G. quadratus share evolutionary traits which allow it to adapt to the conditions in a coastal band of the continental mainland (e.g. Bright 1966, Sherman 2002, Lindquist et al. 2009).

Discussion
On the other hand, the remaining four species of Johngarthia (see López-Victoria and Werding 2008, Hartnoll 2010, Perger et al. 2011 and Gecarcinus ruricola (Bright and Hogue 1972) have been reported from islands only, supporting the pattern suggested by Paulay and Starmer (2011). Several studies strongly indicate that J. planata has not  (Perger et al. 2013;Perger unpubl. data Fig. 2), which agrees with the pattern of mainland absence observed in the four congeners. The ecological flexibility of J. planata, which occurs in habitats ranging from island rainforests to rocky terrain with sparse vegetation (Pérez-Chi 2005, Perger et al. 2013, suggest that the most significant factors which preclude such species from inhabiting the mainland are indeed competition or/and predation (Perger et al. 2013). The presence/absence pattern of J. planata in continental mainland habitats roughly coincides with the replacement of the moist forests of Panama and Costa Rica by dry forests that extend from Nicaragua to Mexico (see Ricketts et al. 1999). The diversity of possible crab predators such as birds (Orme et al. 2005) and mammals (Ceballos and Ehrlich 2006) is lower in the Southern Pacific Dry forest ecoregion than in tropical rainforests of Central America. Whether J. planata appears as well in non-urban areas along the Mexican Pacific coast remains unclear, however, the mainland establishment of such species might be facilitated close to or in urban areas where the lower diversity or/ and abundance of possible predators/competitors is influenced by the presence of humans. Studies from undisturbed forest in the Pacific coast of Costa Rica (Sherman 2002, Griffiths et al. 2007  Further photographs and accounts by Jolley and Brewer (2010) and Brewer (in litt.) indicate that J. planata is a common element of the urban wildlife and seeks food and shelter in closest proximity to human houses: "People who have built homes in the jungle near the ocean, however, consider the allpervasive land crabs quite troublesome. If the crabs can get into the house (they can climb walls!), they can damage clothing, books, and food. Outside of the house, they are quite hard on garden plants, shredding foliage and damaging plant roots from inside their tunnels. By the time November comes, most folks are happy to see the crabs retreat into the ground!" (Jolley and Brewer 2010) These observations demonstrate that human presence does not necessarily have a negative impact on land crabs, as suggested by Paulay and Starmer (2011). The relationship between land crabs and humans might depend on the type of habitat, human settlement system and land use. Exploitation by hunter-gatherers on islands and the introduction of domesticated animals are assumed to have resulted in the extinction of local populations of G. ruricola (Pregill et al. 1988) and a species of Geograpsus (Paulay and Starmer 2011). However, the consumption of land crabs has not been reported from tourist destinations along the Neotropical Pacific coast. As free-roaming domestic animals may be seen as a detriment to tourism (Webster 2013), populations of possible land crab predators/competitors such as pigs, cats, dogs and rats (see Paulay and Starmer 2011) tend to be more controlled than in areas with farmers or hunter-gatherers.
Because gecarcinid land crabs significantly influence tree recruitment by consuming seeds, propagules and seedlings, they are considered important ecosystem engineers (reviewed by Lindquist et al. 2009). While human presence might open a new evolutionary pathway for these otherwise island restricted land crabs, the colonization of continental mainland forests by a large species such as J. planata (see López-Victoria and Werding (2008) for a size comparison) would certainly have profound consequences for the structure and species composition of coastal ecosystems, particularly in view of the possibility that their foraging activity would be less restricted due to lower predation pressure. Further surveys for J. planata and possible crab predators/competitors are needed to determine if the known distributional pattern of such species is the result of human influence.