Brachyuran crabs (Crustacea, Decapoda) from the remote oceanic Archipelago Trindade and Martin Vaz, South Atlantic Ocean Author TAVARES, MARCOS 0000-0002-7186-5787 Museu de Zoologia, Universidade de São Paulo. CEP 04263 - 000, São Paulo, SP, Brazil mdst@usp.br Author MENDONÇA, JOEL BRAGA DE JR. 0000-0002-4593-8495 Museu de Zoologia, Universidade de São Paulo. CEP 04263 - 000, São Paulo, SP, Brazil text Zootaxa 2022 2022-06-02 5146 1 1 129 http://dx.doi.org/10.11646/zootaxa.5146.1.1 journal article 10.11646/zootaxa.5146.1.1 3b24340c-ddcb-45bc-a12b-a3f21832e794 1175­5334 7626155 52C3E5E3-80B6-49DB-BC9C-194560D491F7 Johngarthia lagostoma (H. Milne Edwards, 1837) ( Figs. 46A–I , 47A–G , 48A–F ) Gecarcinus lagostoma H. Milne Edwards, 1837: 27 [ Type locality: Ascension Island ]. Trindade and Martin Vaz specimens. 1 male ( MZUSP 9583 ), Brazil , off Espírito Santo , Trindade Island , Enseada dos Portugueses, M. Tavares and F. W. Kurtz coll., 13.xii.1986 . 1 male ( MZUSP 21430 ), ibidem , Praia das Cabritas , M. Tavares and F. W. Kurtz coll., 13.xii.1986 . 2 parental females each with hatched first stage zoeae ( MZUSP 40221 and 40223), ibidem , 20°30’24’’S , 29°18’57”W , J.B. Mendonça coll., 10.xi.2014 . 1 juvenile male, cl 9.1 mm , cw 10.6 mm ( MZUSP 40322 ), Praia da Tartaruga , 20°31’03.8’’S , 29°18’08.4”W , J.B. Mendonça coll., 10.vi.2012 , at night. 1 female , cl 22 mm , cw 26 mm ; 1 male , cl 30 mm , cw 36 mm ; 1 male cl 32 mm , 38 mm ( MZUSP 40321 ), ibidem , Enseada dos Portugueses , 20°30’27.8’’S , 29°18’50.2”W , J.B. Mendonça coll., 15.vii.2013 . 1 juvenile female, cl 20 mm , cw 23 mm ; 1 juvenile male, cl 22 mm , cw 26 mm ; 1 juvenile male, 1 juvenile female both cl 23 mm , cw 27 mm ; 1 juvenile male cl 28 mm , cw 33 mm ( MZUSP 40352 ), ibidem , 12.vii.2015 . 1 juvenile female cl 14 mm , cw 16 mm ( MZUSP 40226 ), ibidem , J.B. Mendonça coll., 14.ii.2018 . 2 males , 4 females ( MZUSP 22792 ), Trindade Island , Pico do Desejado , TAAF MD55/ Brésil Expedition , M. Tavares coll., 22.v.1987 , altitude around 600 m . 1 male ( MZUSP 17279 ), Martin Vaz Archipelago, 10.x.1988 . Size of largest male: cl 66 mm , cw 79 mm ; largest female: cl 67 mm , cw 76 mm . Comparative material examined. Brazil : 1 male ( MZUSP 36387 ) , 1 female ( MZUSP 3685 ), Rocas Atoll , ii.1972 . 1 female ( MZUSP 30021 ), Fernando de Noronha , Baía dos Porcos , Pedreira do Sueste , 14–16.x.2006 . FIGURE 46. A–I, Johngarthia lagostoma (H. Milne Edwards, 1837) , Trindade Island. A, Pico do Desejado, around 600 m high (July 2018). B, Enseada dos Portugueses. Crabs seeking for food at night near the Brazilian Navy facilitiy (November 2017). C, Retreated to its burrow during the heat hours (December 2017). D, Preying upon a newborn sea turtle at night (May 2012). E, F, Hunting seabirds’ chicks and eggs ( November and December 2017 , respectively). G, Scavenging a carcasse of seabird ( December 2017 ). H, I, Eating leaves o Ipomea ( May 2012 , December 2017 ). Note in (B) two main color morphs (yellow or orange and red or purple); in (G) purple morph. Photographs: (A, C, D, F–I) by J.B. Mendonça, (B, E) by A. Pol. FIGURE 47. A–G, Johngarthia lagostoma (H. Milne Edwards, 1837) . A, F, Male (MZUSP 9583). B–E, G, Male (MZUSP 21430). A, F, Anterior view of body and second pereopod in lateral view, respectively. B, C, Third maxilliped in ventral and dorsal view, respectively. D, E, Second (Mxp2) and first (Mxp1) maxillipeds in dorsal view, respectively. G, Distal part of the first gonopod in pleonal view. Note in (A) Mxp3 gaping noticably, exposing the mandibles; in (B) small palp and small exopodite devoid of flagellum articulating at the ventral side of the merus and basis, respectively; in (D, E) exopodite of Mxp2 and Mxp1 devoid of flagellum; in (G) corneous unguis with subdistal opening. Scales: A, F, 10 mm. B–E, 5 mm. G, 1.5 mm. Distribution. Insular. Rocas Atoll, Fernando de Noronha Archipelago, Ascension Island , Trindade and Martin Vaz Archipelago ( Moreira 1901 ; 1920 ; Lobo 1919 ; Manning & Chace 1990 ). Ecological notes. Johngarthia lagostoma has a high level of independence from the aquatic environment. In Trindade, the crabs are found from upland habitats to heights of 600 m ( Fig. 46A ). The crabs are more active during the night (moonless and dark moons nights are preferred) ( Fig. 46B ), but they are not uncommon during daylight cool hours as well, and usually retreat to their burrows for protection during the heat hours ( Fig. 46C ). The reduction of water loss is a basic requirement for a land crab. In J. lagostoma , the buccal frame is completely covered by the long and broadly operculiform third maxilliped ( Fig. 47A ), whose merus extends anteriorly as far as to cover the remarkably small antenna and antennule, and the palp and maxilliped exopodite (devoid of flagellum) are both reduced in size and articulated at the maxilliped internal face, thus concealed to reduce water loss to a minimum ( Fig. 47B, C ). Additionally, the maxillipeds leave a broad rhomboidal gap when closed, so that food can still enter the mouth and be processed by the mandibles ( Tavares 2002 ) ( Figs. 46D, H ; 47A ). The second and first maxillipeds also have the exopodites devoid of flagellae, which help to minimize water loss ( Fig. 47D, E ). In Trindade, J. lagostoma occasionally visit freshwater streams, some times along with Grapsus grapsus (see Arai et al. 2017 ). Feeding. Johngarthia lagostoma hunts for food, eat green leaves and decaying plant material ( Fig. 46H, I ) (see also Baylis 1915 ), cannibalize conspecifics, and scavenge opportunistically ( Fig. 46G ). It preys upon newborn sea turtles, seabirds’ chicks and eggs ( Fig. 46D–F ), but also upon house mouses when it has the chance. During a Brazilian expedition to Trindade in 1916, a frigatebird endemic to Trindade (see Olson 2017 ) kept alive was killed and eaten by the crabs during the night ( Lobo 1919 ). Visibly, J. lagostoma rely primarily on plant material for food, as also attested by its massive, well calcified gastric mill ossicles (see Lima 2010 ), a feature consistent with the consumption of plant material (see also Linton & Greenaway 2007 ; Allardyce & Linton 2010 ). Breeding behavior. Hartnoll and collaborators contributed a great deal to our knowledge of the breeding behavior and reproduction of J. lagostoma , essentially based on the crab population from the Ascension Island ( Hartnoll et al. 2006 ; 2007 ; 2009 ; 2010 ; 2014 ; Hartnoll 2009 ; 2010 ). The breeding patterns of the crab population from Trindade (this study) is consistent with the patterns described for Ascension and Rocas Atoll ( Teixeira 1996 ), but also show some contrasts as discussed hereafter. In Trindade (this study), mating and egg carrying have been observed from October to November, and hatching from November to December (observations made in 2014 and 2017). In Ascension , scattered data point to breeding migrations occurring from late January to May ( Hartnoll et al. 2006 ; 2009 ; 2010 ). Rodriguez-Rey et al. (2016) using mitochondrial markers found that almost half of the crabs from Trindade had haplotypes exclusive to this island. It is thus tempting to speculate that this might be aided in part by gene flow inhibited through differences in breeding seasons. Both sexes mature by 60 mm to 70 mm ( Hartnoll et al. 2010 ). Males fight each other with their chelipeds to access females ( Fig. 48A ). During the mating, the male is usually under the female (sternum to sternum), which is held tightly by the male’s pereopods ( Fig. 48B ), occasionally by the male’s chelipeds. The strong spines on the male’s pereopods dactyli and propodi help to hold the female in place ( Figs. 47F , 48B ). Both first gonopods are used for sperm transfer during the copulation ( Fig. 48B ). The copulation occurs while the female is in hard-shelled condition either during daylight hours or at night ( Fig. 48B, C ) (see also Hartnoll 2010 ; João et al. 2021 ). The first gonopod is provided subdistally with a corneous unguis with a distal opening ( Fig 47G ). The populations in Ascension , Trindade and Martin Vaz are represented by two color morphs (yellow or orange and red or purple) ( Figs. 46B, G , 48A ) (see also Moreira 1920 ). Coloration is not sex specific. Contrary to Trindade and Ascension , where the pale morph is far more common, 56% of the crabs were red/purple in the Rocas Atoll ( Teixeira 1996 ). Hartnoll et al. (2006) speculated that differently from Ascension , where the pale coloration might be advantageous to survive the long-exposed breeding migration through bare arid lands, such is not the case in the much smaller Rocas Atoll. The long-exposed breeding migration hypothesis is not supported for Trindade, where the pale morph is far more common and there is no breeding migration through particularly arid land extensions. In Trindade (this study) and Ascension ( Hartnoll et al. 2006 ) males and females of both color morphs have been observed copulating with one another. During daylight hours prior to hatching, the ovigerous females remain concealed and do not take food. Near sunset, they migrate towards the beach ( Fig. 48D ), but do not release their larvae until it is dark. Hartnoll et al. (2006) also recorded breeding activity mainly at night on Ascension ( April 2005 ). The ovigerous females enter the sea facing the incoming water (or side on) and release their eggs ( Fig. 48E, F ) by vigorously shaking their body while helding the chelipeds spread out. Females carry about 72,000 eggs in average ( Hartnoll et al. 2010 ). The first zoea stage of J. lagostoma was described only recently ( Colavite et al. 2021 ; Lira et al. 2021 ). In Trindade (this study), spawning migration takes about three consecutive days, the most intenses being the first two days (observations in 2014 and 2017). Egg-laying peaked during the beginning of dark hours (between 6:00 pm and 7:30 pm, Trindade time). Very few males were seen late at night after spawning, but no copulation was observed. In Ascension , males and females migrate but females are far more common. The effect of moonlight and rainfall in the breeding of J. lagostoma is not obvious ( Hartnoll et al. 2006 ). Recruitment. Apparently, the mass recruitment (well documented for other gecarcinids; Hicks 1985 ; Hartnoll & Clark 2006 ) is an exceptional event in J. lagostoma and the effect of the mortality is compensated by the regular trickle recruitment of juveniles. To the best of our knowledge, there is no record in the literature of mass recruitment on Trindade, Rocas Atoll and Fernando de Noronha. The small specimens in Table 4 were probably recruited on Trindade 1–3 years prior to their collection. Recruits are probably naturally infrequent even though they are more cryptic in habitat, hence more easily missed (see also Moreira 1920 ; Hartnoll et al. 2006 ). In Trindade, initial crab stages were found in galleries dug by the adults (observations made in 1987). The mass return to land in J. lagostoma must indeed be an exceptional event, as it was only once ( March 1963 ) recorded on Ascension ( Hartnoll et al. 2006 ). A study based on the examination of a large number of specimens from Ascension revealed very few immature crabs (<cw 60 mm ) suggesting that the crab population on the island is an aging one ( Hartnoll et al . 2009 ). A similar study in regard to Trindade is necessary to provide managers with guidance in setting conservation goals. TABLE 4. Johngarthia lagostoma (H. Milne Edwards, 1837) . Carapace width (cw, in millimeters) of specimens collected on Trindade Island in June 2012, July 2013 and July 2015. For additional details on the specimens see under material examined MZUSP 40322, MZUSP 40321, MZUSP 40352, respectively. MZUSP, Museu de Zoologia, Universidade de São Paulo.

Juvenile male (cw)	Juvenile female (cw)
June 2012	10.6	–
July 2013	–	cw 26
	36	–
	38	–
July 2015	–	23
	26	–
	27	–
	–	27
	33	–

Habitat protection and species conservation. Johngarthia lagostoma is omnivorous but rely heavily on the availability of vegetation for food and, occasionally, for shelter (see above under feeding) ( Fig. 46H, I ). For more than three centuries domestic species introduced into Trindade (e.g. goats, pigs, sheep, donkey, guinea fowl, passerine bird, lizard, cat, mice, some of which became feral) greatly affected the terrestrial biota and reduced the forest cover by more than 80% ( Lobo 1919 ; Oliveira 1951 ; Alves et al. 2011 ). The eradication of most of these domestic species by the Brazilian Navy years ago led to the rapid revegetation. Hartnoll et al. (2006) clarified that the distribution of J. lagostoma in Ascension , normally limited to altitudes above 200 m is essentially the reflection of the subsistence of the vegetation, constrained to higher altitudes by human activities. Clearly, protection of the vegetation in Trindade is a key step towards the protection of J. lagostoma . Predators and symbionts. The Atlantic Lesser Frigatebird, Fregata trinitatis , was observed to drop J. lagostoma from 3–4 m high to break and eat them ( Lobo 1919 ). Baylis (1915) found the oligochaete worm, Enchytraeus carcinophilus Baylis , living in the interior of the gill chamber of J. lagostoma collected between 450 m to 600 m of altitude on Trindade. Manning & Chace (1990) summarized the scattered information accumulated for J. lagostoma in Ascension since Darwin (1839) . Remarks. H. Milne Edwards (1837: 27) described Johngarthia lagostoma (as Gecarcinus lagostoma ) upon material presented by Quoy and Gaimard and gave “l’Australasie” as the type locality (Jean Ren Constant Quoy and Joseph Paul Gaimard were naturalists aboard the voyage of the “L’Astrolabe”). H. Milne Edwards also described the Indo-West Pacific Gecarcoidea lalandii and stated “ Brésil ” as the type locality. This mistake was previously identified by several authors. Judging from H. Milne Edwards’ (1837) statement (viz. “ Brésil ”), Trindade was likely candidate for the type locality of J. lagostoma as L’Astrolabe is known to have approached this island. However, according to L’Astrolabe’s commander Dumont D’Urville the expedition actually never landed in Trindade: “J’avais le dessein de tenter une excursion à la côte [of Trindade] avec les naturalistes; mais le ressac y était si violent, et la mer brisait avec tant de fureur sur tous ses points, que je ne jugeai pas à propos d’y hasarder une embarcation.” ( Dumont D’Urville, 1830: 70 ). Indeed, the vessel departed from Toulon on 22 April 1826 but contrary winds delayed the expedition so long that L’Astrolabe approached Trindade only three months later, on 31 July. From there, L’Astrolabe sailed non-stop to Port du Roi Georges (currently Albany, western Australia) where it arrived on 7 October. In her way back to France in 1829, L’Astrolabe stoped at the Ascension Island where numerous natural history specimens were collected ( Quoy & Gaimard, 1833 ), among which possibly the material used by H. Milne Edwards (1837) in the original description of J. lagostoma . Therefore, we agree with Manning & Chace’s (1990) suggestion that Ascension is most probably the type locality of J. lagostoma .