Aspects of the natural history of Phrynus barbadensis ( Pocock , 1893 ) ( Amblypygi : Phrynidae )

Information on preys and predators of the amblypygids is scarce, largely disperse and sometimes overlooked by the arachnologist. Phrynus barbadensis is a Neotropical whip spider widely distributed, but its natural history is poorly known. The main purpose of this contribution deals with preys, predators, reproductive effort and microhabitat preferences of P. barbadensis in a Colombian locality. Field work was carried out by two researchers during four expeditions of six days each, between June and November 2017. Two observed cases of intragremial predation concerned to the spitting spider Scytodes longipes Lucas (Araneae: Scytodidae) and the giant whip spider Heterophrynus caribensis Armas, Torres-Contreras & Álvarez (Phrynidae: Heterophryninae). A new case of a mollusk as prey of whip spiders is also recorded. The number of embryos per batch in P. barbadensis was 14-79 (n = 27, mean = 40, standard error = 3.83), having a positive correlation with the female size. This species was highly associated to fallen trunks and rocks, but poorly to the litter and rocky walls (χ2 = 16.26, P < 0.001); with respect to the substrate temperature, it showed a positive association. The cannibalism and necrophagy among the whip spiders are briefly commented, and updated lists of the known preys and predators of the amblypygids are also provided.


Study site
The field work was conducted in Montes de María (09°31' N; 75°20' W -250 m a.s.l.), Colosó municipality, Sucre department, Colombia.This is a tropical dry forest, in a mountainous landscape with primary forest and several springs.The annual mean temperature is 26.8 °C, the precipitation varies between 1000 and 1200 mm and the relative humidity is 77% (Aguilera, 2005).

Sampling
The field work was carried out between 19:00 and 23:00 h by two researchers, during four expeditions of six days each, from June to November, 2017.To determine the reproductive effort, 27 ovigerous females of P. barbadensis were collected.Four microhabitats (rocks, fallen trunks, crevices in rocky walls, and litter) were manually examined randomly searching for whip spiders.The sampling effort were distributed evenly with 20 minutes for each microhabitat.Temperature of the substratum was assessed by means a Thermoworks 24-inch waterproof digital thermometer.
All the specimens were preserved in ethanol 75%.Voucher specimens are deposited in the Zoological Museum of the University of Sucre, Colombia (MZUSU) with the collection number MZUSU-I00001, MZUSU-I00002, MZUSU-I00003, MZUSU-I00004, MZUSU-I00005.The specimens were collected within the framework permission for the collection of specimens of wild species of biological diversity for the purpose of scientific research granted by the National Environmental License Authority (ANLA) to the University of Sucre.

Statistical analyses
Carapace length was used as a measure of size of specimens and, a correlation analysis of Spearman was applied by means of the software PAST version 3.14 (Hammer et al., 2001).
To determine microhabitat preference, an analysis of binary logistic regression was applied in function of the substratum temperature, by means of the software SPSS version 22 for Windows (IBM, Armonk, NY, USA).A test of homogeneity ( χ 2 ) was applied to reject the null hypothesis of similar preference of microhabitat by this species, assuming that all the microhabitats had the same probability of being occupied.
Under particular conditions, intraguild predation, including cannibalism, might play an important role in the trophic structure of those ecosystems in which the whip spiders are abundant (Chapin & Hebets, 2016).Although field studies on this ecological aspect have not been conducted, sporadic observations seem to reinforce this hypothesis, but this does not constitute a high criterion.
Phrynus barbadensis is a phrynid species well represented in the Colombian Caribbean (Chiriví-Joya & Armas, 2012).In recent years, some aspects of its natural history have been documented (Chiriví-Joya & Armas, 2012;Torres-Contreras et al., 2015).In the present contribution, additional preys and predators of this whip spider are documented, as well as data on its habitat preferences and reproductive biology.

RESULTS
Predation by Scytodes longipes (Fig. 1A, Table I) On Oct 18 th , 2017, a spitting spider Scytodes longipes (Araneae: Scytodidae) was found underneath a rock feeding on the whip spider P. barbadensis.The spider was an adult female (total length: 9.95 mm, prosoma length: 4.15 mm).The whip spider was an adult female (total length: 9.42 mm, carapace length: 3.64 mm).At the moment of the observation, the whip spider was entangled in the web and wrapped by silk on the pedipalps and prosoma, and the spider begun to feed on it.
Predation by Heterophrynus caribensis (Fig. 1B,  Table I) On Aug 26 th , 2017, an adult female of H. caribensis (total length: 21.8 mm, carapace median length: 4.8 mm) was found on a rock eating a female P. barbadensis (total length: 15 mm, carapace median length: 2.6 mm).At the time of the observation, the predator strongly held the whole body of the prey while consuming its opisthosoma.The individual of P. barbadensis was still fresh from an ecdysis.
Predation on a gastropod mollusk (Fig. 1C, Table II) On Sept 11 th , 2017, an adult female of P. barbadensis (total length 15.59 mm, carapace median length 5.21 mm) was found under a stone eating a gastropod mollusk.At that moment, the amblypygid grasped with its pedipalps and chelicerae the soft corporal mass of the mollusk.The shell was empty, with a small rupture in its aperture.Measurements (in millimeters) of the shell were as follows: total length: 6.83, width: 4.64, aperture: 2.59 x 1.94.
Two cases of cannibalism in Heterophrynus guacharo Armas, were reported by Morales-Álvarez & González (1986), but they did not provide additional details.A similar situation occurs with the intraguild predations recorded by Armas (1995), Gering (in Hebets, 2002) and Chapin (2011).Based on the exiguous available data (Armas & Ramirez, 1989;Armas et al., 2013;Teruel & Toledo, 2014;this paper), only two preliminary conclusions may be addressed: (1) size differences determine amblypygid-amblypygid and other arachnidamblypygid predation, being the larger individuals the predators; (2) as in other arthropods, the ecdysis and its immediately posterior process of sclerotization represent a hard phase in which the whip spiders are dramatically exposed to predators.Those conclusions are congruent with some results obtained by Polis (1981) and Polis & McCormick (1981) in several North American scorpions.
Certainly, intraguild predation and cannibalism offer remarkable opportunities to understand the dynamic relationships within an ecosystem.Nevertheless, as already pointed out, most existing information on whip spider's predators result of opportunistic field observations, and quantitative assessments of their role as protagonist in the ecosystem trophic structures are lacking (Chapin & Hebets, 2016).

Preys
Amblypygids are generalist pantropical arachnids, seemingly opportunistic (Chapin & Hebets, 2016), but it is obvious that our present knowledge on its preys is meager.Remarkable or curious field observations on the natural history are sometimes totally or partially omitted, mainly because the principal interest had been focused on the taxonomy.In the future, as a result of more detailed researches, perhaps some food items of the amblypygid diet might be not as uncommon as considered at this moment.

TORRES, R.A. et al. Natural history of Phrynus barbadensis
Table II (cont.).Known preys of the amblypygids Field observations only.Amblypygid-amblypygid predation is excluded (see Table I) Spiders are mentioned as predated by three amblypygid species, but in the case of C. israelensis, only the immature individuals of Loxosceles spp.were consumed (G.Wizen, pers.com., Nov 27 th , 2017).
Terrestrial isopods are recorded as eaten by three species (Table II), but C. israelensis was observed that predated on a small-sized isopod species (up to 7 mm in length) in all parts of the cave, mainly on the vertical walls; also, a single adult C. israelensis eaten on a larger isopod (15 mm in length), that seemingly entered the cave from the outside (G.Wizen, pers.com., Nov 27 th ,  2017).
With respect to the necrophagy, Peck (1974) reported it for P. longipes (that he identified as Tarantula fuscimana) from Aguas Buenas Cave, Puerto Rico, but this interesting record has been overlooked by posterior researchers, excepting Moyá-Guzmán (2009).Armas & Abreu-Collado (1999) 2017) reported bat necrophagy by the large South American amblypygid Heterophrynus longicornis Butler.Now, it is out of any doubt that necrophagy might be a frequent behavior in natural populations of some whip spiders.

Reproductive effort
Chiriví-Joya & Armas (2012) mentioned a Colombian female of P. barbadensis (carapace median length 7.3 mm) that carried 27 embryos, similar to what was found in this work.For this species, Quintero (1981) recorded 9 to 24 eggs or embryos per batch, but its correlation with any morphometric variable was not explored.Positive correlation of the clutch size and the female length was also found by Weygoldt (2000) and Armas & Pérez-González (2001) in three Caribbean Phrynus species, although a linear relationship is not always present (Weygoldt, 2000).

Microhabitat preference
High association of P. barbadensis with decaying trunks and rocks seems to be in correspondence with the usually humid and temperate condition of these microhabitats, excellent food source, availability of daytime shelters and appropriate places for reproduction.Although cannibalism occurs (Torres-Contreras et al., 2015), it is common to find several individuals in the same decaying trunk, usually interacting with each other.
Microhabitats as vertical structures (trees and rocky walls) are infrequently used by P. barbadensis, mainly because these sites are mostly occupied by H. caribensis, a potential predator.Some species of the genus Phrynus are usually associated with large trees bearing buttresses (Hebets, 2002;Bloch & Weiss, 2002), but they are the biggest amblypygids in those places.Large South American species of the genus Heterophrynus also occur in similar microhabitats (Weygoldt, 1977;Dias & Machado, 2006;Chapin, 2014).

Fig. 1 .
Fig. 1.Feed interaction in Phrynus barbadensis.A, predatation by Scytodes longipes and B, by Heterophrynus caribensis.C, eating a gastropod mollusc (Ampullaridae).Photos by Richard A. Torres Fig. 2. A) Positive correlation between the carapace median length (X axis) and the clutch size (Y axis).B) Model of microhabitat selection of Phrynus barbadensis in a Colombian locality, based on substrate temperature.
mentioned for the same species a similar case observed in a Hispaniolan cave [it was mentioned with some doubt by Armas & Pérez-Gonzalez (2001) and Armas (2006)].A few years later, García-Rivera et al. (2009) recorded three specimens of the Cuban large amblypygid Paraphrynus robustus Franganillo, eating on two dead bats, and recently, Prous et al. (