2002. The Journal of Arachnology 30:613±617

SHORT COMMUNICATION

FEEDING IN MAXCHERNES IPORANGAE (PSEUDOSCORPIONES, CHERNETIDAE) IN CAPTIVITY

Renata de Andrade and Pedro Gnaspini: Departamento de Zoologia, Instituto de BiocieÃncias, Universidade de SaÄo Paulo, Caixa Postal 11461, 05422-970 SaÄo Paulo, SP, Brazil. E-mail: [email protected]

ABSTRACT. The feeding behavior of the cave Maxchernes iporangae Mahnert & An- drade 1998 was studied in the laboratory. We also investigated aspects such as preference and frequency. Nymphs are more active in prey capture. Cannibalism is uncommon. The frequency of feeding of adults was about once a month, with an increased rate for females during the reproductive period. Keywords: Pseudoscorpiones, feeding behavior, feeding frequency, Chernetidae, Maxchernes

Pseudoscorpions are predators of other arthro- givorous bat guano piles from Alambari de Baixo pods. The organisms consumed by Cave (SP-012, 24Њ33Ј15Љ S and 48Њ39Ј55Љ W), sit- kept in captivity included larvae and adults of Dro- uated in the Ribeira River Valley (SaÄo Paulo State, sophila sp. (Gilbert 1951; Levi 1953; Goddard Brazil). This species seems to be restricted to this 1976), Isoptera (Brach 1978; Hahn & Matthiesen kind of guano in this particular cave (Mahnert & 1993a), Collembola (Wood & Gabbutt 1979a, Andrade, 1998; pers. obs.). Collections and obser- 1979b; Johnson & Wellington 1980), Psocoptera vations were made between February 1996 and (Levi 1948, 1953), and larvae and adult of cucujid February 1998. and tenebrionid beetles (Levi 1948, 1953). Infor- The pseudoscorpions were placed with guano in mation about pseudoscorpion prey and predators small closed containers and transported to the lab- can be found in Jones (1975). oratory, where some pseudoscorpions were kept in Chthoniidae, Neobisiidae and some related fam- groups (up to 18 individuals) in transparent plastic ilies masticate the prey with their chelicerae; at the boxes (9 cm lengthx6cmwidth x 2.5 cm height). same time the food is digested by a ¯uid from the Others were kept individually in glass Petri dishes oral cavity. Later, the digested contents are ingested (2.5 cm diameter x 1.5 cm height). All containers (Gilbert 1951; Weygoldt 1969). Other groups (e.g., contained moistened guano or ®ne sand on the bot- Olpiidae, Garypidae, and all Cheliferoidea) use the tom, and were kept under almost constant darkness chelicerae to make a hole in the body wall of the and at a temperature of 21.0 ЊC Ϯ 2.0. This tem- prey, through which an enzymatic ¯uid is injected. perature is similar to the temperature of the cave The digested contents are then ingested (Feio 1942; inhabited by the species studied. Regarding the use Gilbert 1951). After digestion, the ingested material of alternative substrates, we preferred the use of that has not been used is transformed into crystals, guano. However, this material rots with time and probably guanine (Gilbert 1952), which is stored in accumulates fungi, needing to be replaced. Because the rectal pocket and excreted from time to time. A sometimes it was not available at the laboratory, we comprehensive review of the digestive tract and nu- used ®ne sand. trition of pseudoscorpions is given in Heurtault In order to analyze the feeding frequency, the (1973). pseudoscorpions were fed twice a week. Each iso- The present study gives further information about lated adult received one live adult of Drosophila feeding in pseudoscorpions, speci®cally regarding sp. (slightly larger than an adult M. iporangae). Af- feeding behavior, preference and frequency in the ter six hours, the dish was examined. The feeding chernetid pseudoscorpion Maxchernes iporangae was considered effective if the pseudoscorpion was Mahnert & Andrade 1988, a species living in a sub- found eating the prey. Other items were also offered terranean habitat. to adults: psocopterans, tineid moth larvae, psy- Individuals of Maxchernes iporangae, which are chodid dipterans, collembolans, Endecous sp. crick- approximately 2 mm in length when adults (see et nymphs (which occur in the same cave as the Mahnert & Andrade 1998), were collected on fru- pseudoscorpions) and isopods (from the same gua-

613 614 THE JOURNAL OF ARACHNOLOGY no piles as the pseudoscorpions). The last two an- aspect, frequently observed in grouped pseudoscor- imals were offered to determine if they could be pions, was practically absent among isolated pseu- natural prey of M. iporangae. The other doscorpions. This behavior may represent a re- were offered because they were available in the lab- sponse to the recognition of other pseudoscorpions oratory, although they did not occur in the caves in proximity and may avoid prey theft by another studied. The initial purpose of trying different food pseudoscorpion. items was to maintain the pseudoscorpions in the The sharing of prey by up to three pseudoscor- laboratory, since the cave is located 5 hours from pions was observed among pseudoscorpions kept in SaÄo Paulo, because the original objective of the groups. On these occasions, the pseudoscorpions study was to follow their life cycle. Nymphs were were suf®ciently separated so that they did not initially offered live Drosophila sp. larvae. Later, a touch each other. However, if some disturbance oc- dead adult Drosophila sp. was left in each Petri dish curred, such as prey movement or the approach of with nymphs. More than thirty observations on another individual, the pseudoscorpions became ag- feeding behavior were performed with isolated and/ itated, attacking each other, without releasing the or grouped pseudoscorpions. prey and pulling on it, until one individual suc- Voucher specimens, collected at the same guano ceeded in moving off with the prey. The partition deposit where the type specimens were collected, of prey was earlier recorded for nymphs and adults are deposited at the Museu de Zoologia da Univ- of Paratemnoides elongatus (Banks 1895) (Atem- ersidade de SaÄo Paulo, SaÄo Paulo, Brazil (MZSP). nidae), however, without aggressive interactions or Feeding behavior.ÐAdults of M. iporangae attempts to take the prey (Brach 1978). moved relatively slower than nymphs and mostly Grooming behavior was often observed. The attacked prey by quick movements of the pedipalps most important grooming organ is the serrula ex- when the prey was near. The nymphs attacked prey terior of the movable ®ngers of the chelicerae more readily, pursuing prey over relatively longer (Weygoldt 1969). In M. iporangae the palpal ®n- distances. Protonymphs were more active in prey gers were cleaned by drawing them through the capture than later instars. This was also observed chelicerae; the chelicerae were cleaned by rubbing for Paratemnoides minor (Balzan 1892) (Atemni- each other; and the palpal coxae by cheliceral rub- dae) (see Hahn & Matthiesen 1993a) and is prob- bing. The grooming occurred just after the prey was ably related to the larger feeding needs of the placed in the dish with the pseudoscorpion, during young, in order to allow faster growth and devel- and at the end of feeding, after the prey was re- opment. leased. The grooming of the palpal ®ngers before Maxchernes iporangae grasped the prey with the feeding, when the prey was placed in the dish, palpal chelae and immobilized it with their poison. would possibly have the function of improving the The time taken to paralyze the prey varied. The capacity of recognition and detection of the prey time in which the pseudoscorpion kept the prey be- and its location by using the palpal trichobothria. tween the palpal chelae also varied, reaching up to Such behavior is usual in other species of pseudo- 10 min. In some cases, the grasped drosophilid was scorpions (Weygoldt 1969; Heurtault 1973). immobilized in a few seconds, in others, it took Feeding preference.ÐWhen live ¯y larvae longer. Probably the immobilization time is related (Drosophila sp.) were offered as food to proto- to the prey region pierced (Feio 1942), and/or to nymphs of M. iporangae that hatched in captivity, the prey sensitivity and size. After immobilization, only two attacks were observed. The protonymphs the prey was passed to the chelicerae, where it re- only pinched the prey by quick movements of the mained for a variable time, sometimes exceeding pedipalps, without taking the prey. The same hap- 2.5 h. On some occasions, the pseudoscorpions pened with small collembolans, except on one oc- were observed piercing a prey in different positions, casion, when a protonymph grasped and passed it a behavior also recorded for Dactylochelifer latreil- to the chelicerae. lei (Leach 1817) (Cheliferidae) by Gilbert (1951). Prey rejection probably was the main cause of This behavior allows more ef®cient utilization of the low survival rate (4%) observed among proto- the prey by feeding at multiple points. nymphs, which is considered to be the more active During feeding, the prey was held only by the metabolic instar in many species of pseudoscorpi- chelicerae, and the palps were kept free and direct- ons that possess a free protonymph phase (Levi ed laterally, in a characteristic defensive posture, as 1948, 1953; Goddard 1979; Hahn & Matthiesen observed for other pseudoscorpions (Gilbert 1951; 1993a). Weygoldt 1969). The palps were used to attack oth- Good survival rates (increased from 4% to 40%) er pseudoscorpions that occasionally approached. were obtained when dead adult ¯ies were placed in Individuals of M. iporangae were often observed the dishes with protonymphs. Although the prey walking with prey held in their palps or even by was large and feeding was rarely observed, the the chelicerae, until they found a secure or hidden mortality rate of these protonymphs decreased, in- place, where they stopped and started feeding. This dicating that the nymphs were probably feeding. In ANDRADE & GNASPINIÐFEEDING BEHAVIOR OF MAXCHERNES 615 addition to drosophilids, deutonymphs and trito- (Cheliferidae). Varied results occurred among nymphs accepted other food, such as tineid larvae Atemnidae: Paratemnoides elongatus did not show and psocopterans. Adult pseudoscorpions accepted cannibalism (Brach 1978), whereas P. minor (Hahn ¯y larvae in addition to dead or live adult ¯ies, but, & Matthiesen 1993b) did. in that case, at a lower frequency than the accep- We observed only three cases of cannibalism in tance of adult ¯ies. Many times they only pinched M. iporangae, all three with alternative food (¯ies) the prey without grasping it, then rejected the food available. First, a protonymph fed on a second pro- offered. Other prey accepted were psychodid dip- tonymph kept in the same Petri dish. The victim terans, psocopterans and tineid larvae, the later in was inside its molting chamber, in a characteristic higher frequency than the former. We should stress torpid condition that precedes the molt, thus unable that psocopterans and tineid moths are common in to move or defend itself. On another occasion, an guano deposits, even in similar frugivorous bat gua- adult female was observed preying on a recently no (such as in Casa de Pedra caveÐsee Gnaspini hatched protonymph. Considering that we had 12 1989a, b), but not in this guano pile, so far. Collem- breeding females with a total of 118 hatched bolans were not taken, which is probably related to nymphs, it gives a rate of less than 1% cannibalism. the collembolan's agility. The possible natural prey Finally, a female was found feeding on her brood (Endecous nymphs and isopods) were not taken at sac, which was previously abandoned outside the all. nest at an advanced stage of development. Consid- On one occasion, in the ®eld, a pseudoscorpion ering that she did not abandon her eggsac to spe- was observed dragging a prey with its palp. Both ci®cally feed upon it (she probably found the eggs- were collected and brought to laboratory where the ac by chance), and that we do not know if females pseudoscorpion was identi®ed as an adult male and can recognize abandoned brood sacs as their own, the prey as an early nymph of an undetermined spe- we can not even assure that this is a case of inten- cies of seed bug (Heteroptera, Lygaeidae). The oc- tional cannibalism. The last two cases occurred with currence of nymphs and adults of two undetermined adults kept individually (from other adults, but not species of the family Lygaeidae inhabiting guano from their own brood). In general, cannibalism can piles of frugivorous bats in the Alambari de Baixo be considered uncommon in M. iporangae, espe- Cave was recorded by Gnaspini-Netto (1989a, b). cially considering that (1) it did not occur among These heteropterans were considered by Gnaspini adults kept in groups, and (2) it was recorded only (1992) to be guanobites, a word used to de®ne or- three times (ca. 1%) over 310 observations done for ganisms which, in caves, inhabit guano deposits ex- M. iporangae during this study. clusively, where they complete their life cycle. Be- Feeding frequency.ÐGenerally, adult pseudo- cause of the preying event directly observed in the scorpions of M. iporangae ate about once a month. ®eld and because of the probable restriction (con- The average number of prey eaten per month was sidering the cave population) of these bugs to the 1.14 Ϯ 0.50 s.d. (n ϭ 47). There are few studies on same guano piles where M. iporangae is present feeding frequency of other pseudoscorpions. For (Gnaspini & Trajano 2000), it is probable that these comparison, Levi (1948) reported that adults of bugs are one (and maybe the principal) of the nat- Chelifer cancroides can feed once or twice a week. ural prey of this species. Unfortunately, it was not When sexes were analyzed independently, the possible to offer these animals to pseudoscorpions monthly average feeding frequency of females of in captivity. M. iporangae was 1.27 Ϯ 0.50 (n ϭ 33); and of There are few studies concerning feeding pref- males was 0.83 Ϯ 0.34 (n ϭ 14). We observed that erence of pseudoscorpions. Weygoldt (1969) re- 85% of males had a feeding frequency between ported that chernetids prefer insects, such as small 0.4±1.19, whereas in 75% of females the frequency dipterans, psocopterans and beetles, and that many was between 0.8±1.99 times a month. Although the species can be maintained on drosophilids, as we con®dence interval for feeding frequency of males did with the studied species. and females overlap, Mann-Whitney rank sum test Cannibalism.ÐWeygoldt (1969) considered (T ϭ 213.0, P ϭ 0.004) showed that the sexual cannibalism to be a rare event among pseudoscor- difference between frequencies is statistically sig- pions, and that it would occur among animals kept ni®cant. In addition, the monthly average feeding in captivity without food for a long time, especially frequency of females after breeding increased to considering that older or injured animals could be 1.50 Ϯ 0.27 (n ϭ 11), but this increase is not sig- attacked by others. Considering chernetids, Levi ni®cant (overlap of con®dence intervals and Mann- (1953) did not observe cannibalism among individ- Whitney rank sum testÐT ϭ 263.0, P ϭ 0.222). uals of minor Hoff 1949 kept in The energy spent for the nutrition of embryos and captivity. On the other hand, considering other for the time spent inside nest chambers may be re- Cheliferoidea (in which Chernetidae is included), sponsible for the increase (although not signi®cant) Levi (1948) observed cannibalism among proto- in feeding frequency of females in the reproductive nymphs of Chelifer cancroides (Linnaeus 1758) period. This is also common in other that 616 THE JOURNAL OF ARACHNOLOGY spend some time with their brood without feeding Gnaspini-Netto, P. 1989b. Fauna associated with bat (e.g., laniatorean harvestmen, Gnaspini 1995). guano deposits from Brazilian caves (a compar- Similarly, an increase in the feeding activity of ison). Pp. 52±54. In Proceedings of the Interna- animals having recently left molting chambers was tional Congress of Speleology, 10, Budapest, observed in two cases. The monthly average feed- Hungary. ing frequency of a recently molted adult female was Gnaspini, P. 1992. Bat guano ecosystems. A new 3.7 during the three months subsequent to exiting classi®cation and some considerations with spe- the molting chamber. The second case is a trito- cial references to neotropical data. MeÂmoires de nymph, which increased its feeding frequency to BiospeÂologie 19:135±138. 2.0 also for three months. It is expected that pseu- Gnaspini, P. 1995. Reproduction and postembryonic doscorpions increase their feeding frequency after development of Goniosoma spelaeum, a cavernic- the molt, due to having spent a long time without olous harvestman from southeastern Brazil (Arach- food. This increase is expected to be larger in early nida: Opiliones: Gonyleptidae). Invertebrate Repro- stages because they are more active and feed more duction and Development 28(2):137±151. frequently (Levi 1948; Hahn & Matthiesen 1993a). Gnaspini, P. & E. Trajano. 2000. Guano communi- The fact that our observations do not agree with ties in tropical caves. Case Study: Brazilian this statement is probably due to the extremely low Caves. Pp. 251±268 In Wilkens, H., D.C. Culver number of cases observed. & W.F. Humphreys (Eds.), Ecosystems of the An ecological study focusing on this species in WorldÐSubterranean Biota. Elsevier, Amster- the ®eld is presently being conducted by the senior dam. 791p. author, including food preferences, and should give Goddard, S.J. 1976. Feeding in Neobisium musco- additional information that could resolve some un- rum (Leach) (Arachnida: Pseudoscorpiones). answered questions. Bulletin of the British Arachnological Society 3(8):232±234. ACKNOWLEDGMENTS Goddard, S.J. 1979. The population metabolism and We thank Instituto Florestal de SaÄo Paulo for allow- life history tactics of Neobisium muscorum ing studies at Parque Estadual TurõÂstico do Alto Ri- (Leach) (Arachnida: Pseudoscorpiones). Oecol- beira. We also thank Dr. S. Hoenen (IBUSP), the edi- ogia 42:91±105. tors and the reviewers, Drs. V. Mahnert and R.B. Pape, Hahn, N.S. & F.A. Matthiesen. 1993a. Desenvol- for their valuable comments on the manuscript. This vimento poÂs-embrionaÂrio de Paratemnus minor study is part of a project supported by a M.Sc. fellow- (Pseudoscorpiones, Atemnidae). Revista Brasi- ship from FAPESP (FundacËaÄo de Amparo aÁ Pesquisa leira de Biologia 53(3):345±353. do Estado de SaÄo Paulo), # 96/5520±5, Brazil, for the Hahn, N.S. & F.A. Matthiesen. 1993b. Notas biol- senior author. The junior author has a research grant oÂgicas sobre Paratemnus minor (Pseudoscorpi- FAPESP # 00/04686±4 and a research fellowship from ones, Atemnidae). Revista Brasileira de Biologia CNPq (Conselho Nacional de Desenvolvimento Cien- 53(4):571±574. tõ®co e TecnoloÂgico), # 300326/94±7, Brazil. Heurtault, J. 1973. Contribution aÁ la connaissance biologique et anatomo-physiologique des Pseu- LITERATURE CITED doscorpions. Bulletin du MuseÂum National d- Brach, V. 1978. 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