ADULT -JUVENIL E ALIMENT ARY RELATIONSHIPS IN (COLEOPTERA)

JoRGE E. V ALENZUELA-GONZALEZ

Instituto de Ecología. A. C Apartado PP<,tal No. 63 91000 X a lapa. Veracruz y Centro de Investigaciones Ecológicas del Sureste Apartado Postal No. 36 30700 Tapachula. Chiapas MFXICO

Folia Entomolrígica A1c\imna No. 85. 25-37 (1992)

Rcccivcd fnr puhlic.llion btllJ:Ir\ 2h. ¡qq_• Acn·pt,·d f,ll. puhliL:!Iinll !uil 1..! lli'l2 26 FOLIA ENTOMOL. MEX. 85 (1992) V ALENZUELA: ALIMENTAR Y R

ABSTRACT INTROD

The reBults reported in this paper show that !luvae of passa.lids are unable to feed directly from wood. Their main BOUree of food is a mixture of adult faeces and powdered wood Parental behaviors in Passalids in fragments produced by adults during galleries excavation. Newly emerged adults are also eggs, 2) excavation of galleries, 3) pu unable to use wood as their souree of food unless they have previously ingest faeces from older several aspects of the biology and beh adults. This fact suggests the existence of a symbiotic relationship with rnicroorganisms for 1932; Gray, 1946; Reyes-Castillo, degradation and/or assimilation of wood in adults. On the other hand, 1 also found that, usually, Schuster, 1985; Reyes-Castillo adult faeces has a higher nitrogen concentration than ingested wood. In larvae faeces, this & phenomenon may also take place but less frequently; besides, increases tend to be considerably Castillo, 1985; Valenzuela-Gonzalez & less than with adults. Differences found between larvae and adults regarding their ability to use 1986a, b). wood for feeding are probably dueto sorne important variations existing in their digestive tracts. The main difference concems the existence, in aduts, of a structure that could be a fennentation The nature of the interactions be chamber; this structure is absent in larvae. The importance of these alimentary relationships, nutrition, has not been well elucidatec in regard to the evolution of social bchavior in passa.lids, is discussed. food for Passalids is a mixture of KEY WORDS: Passalidae, Coleoptera, Parental Behaviors, Subsocial Behavior, Nutrition, during gallery excavation and faeces (1 Xylophagy. Castillo & Halffter, 1984; Valenzuel constantly compressed by adults again RESUMEN lined with this mixture.

Los resultados reportados en este trabajo muestran que las larvas de los pasálidos son Ohaus (1900, 1909) was the first t1 incapaces de alimentarse directamente de la madera. Su fuente principal de alimentación es una for their feeding, due an insufficie1 mezcla de excrementos de adultos y fragmentos de madera producidos durante la excavación de las galerías. Los adultos recién emergidos tampoco pueden sobrevivir con una dieta a base xylophagous nutrition. More recently de madera si no tienen la oportunidad de ingerir, previamente, excrementos de otros adultos. have a mandibular force that is far ~ Estos resultados sugieren la existencia de relaciones simbióticas con microorganismos para la Castillo & Jarman, 1981; Jarman & degradación de la madera en los adultos. Se encontró también que los excrementos de los could give sorne support to Ohaus' adultos poseen, generalmente, un mayor contenido de nitrógeno que la madera de que se reported that the larvae's mandibules 1 alimentan. Este mismo fenómeno ocurre en los excrementos de las larvas, pero con menor frecuencia que en los adultos; por otra parte, dichos incrementos son considerablemente mayores he claimed that, concerning their fe1 en el caso de los adultos que en el de las larvas. Estas diferencias entre larvas y adultos, adults. Pearse et al (1936) and ( concernientes a su capacidad de poder aprovechar la madera cpmo fuente de alimentación, observations, but their results are inc1 probablemente sean originadas por las variaciones existentes en sus tubos digestivos. La of adults in larvae nutrition. Finally, diferencia principal radica en la presencia de una estructura, que probablemente funciona como Odum (1969) showed the importance una cámara de fennentación, en el intestino de los adultos; dicha estructura no existe en las larvas. Por último, se discuten algunos aspectos de la importancia que la xilofagia puede haber tenido en la evolución del comportamiento social en estos insectos. Concerning the participation of syn ofthese , Lewis (1926) and Pea PAlABRAS CIA VE: Passulidue, Colcoptcrn, Comportamientos Parentales, Comportamiento for cellulotic protozoires in the gut Subsocial, Alimentación, Xilofagia. However, jt is well known that bacteri intestines of Passalids, but it is unkr participation in the nutrition of thes Heymons, 1934; Patterson, 1937; Lh -fOL. MEX. 85 (1992) VALENZUELA: ALIMENTARY RELATIONSHIPS IN PASSALIDAE 27

~BSTRACT INTRODUCTION

" that larvae of passalids are unable to feed directly ia a mixture of adult faeces and powdered wood Parental behaviors in Passalids include: 1) care and protection of the lcrica cxcavation. Newly emerged adults are also eggs, 2) excavation of galleries, 3) pupal cell building and 4) feeding. (For unlesa thcy havc previously ingest faeces from older several aspects of the biology and behavior of the group, see: Miller, 1931, r a aymbiotic rclationship with microorganisms for 1932; Gray, 1946; Reyes-Castillo, 1970; Schuster, 1975; Schuster & adults. On the other hand, 1 also found that, usually, llration than ingested wood. In larvae faeces, this Schuster, 1985; Reyes-Castillo & Halffter, 1984; Jarman & Reyes­ rcquently; besides, incrcases tend to be considerably Castillo,1985; Valenzuela-Gonzalez & Castillo, 1984; Valenzuela-González, :ween larvae and adults regarding their ability to use 1986a, b). important variations existing in their digestive tracts. , in aduts, of a structurc that could be a fennentation The nature of the interactions between adults and young, concerning . The importance of these alimentary relationships, •r in passalids, is discussed. nutrition, has not been well elucidated yet. Apparently, the main source of food for Passalids is a mixture of powdered wood fragments produced Parental Behaviors, Subsocial Bchavior, Nutrition, during gallery excavation and faeces (Pearse et al, 1936; Gray, 1946; Reyes­ Castillo & Halffter, 1984; Valenzuela-González 1986a); these detritus are constantly compressed by adults against the gallery walls, which are usually ESUMEN Iined with this mixture.

111jo muestran que las larvas de los pusálidos son Ohaus (1900, 1909) was the first to propose that larvae depend on adults 1nadera. Su fuente principal de alimentación es una entos de madera producidos durante la excavación for their feeding, due an insufficient adaptation of their mandibules to

)1 tampoco pueden sobrevivir con una dieta a base xylophagous nutrition. More recently, sorne studies have shown that adults tgerir, previamente, excrementos de otros adultos. have a mandibular force that is far superior to that of the larvae (Reyes­ elaciones simbióticas con microorganismos para la Castillo & Jarman, 1981; Jarman & Reyes-Castillo, 1985), a fact which Se encontró también que los excrementos de los could give sorne support to Ohaus's ideas. However, Heymons (1929) rontenido de nitrógeno que la madera de que se reported that the larvae's mandibules were well-adapted for this regime, and n los excrementos de las larvas, pero con menor dichos incrementos son considerablemente mayores he claimed that, concerning their feeding, larvae were independent from 1 larvas. Estas diferencias entre larvas y adultos, adults. Pearse et al (1936) and Gray (1946) made sorne additional ovechar la madera cpmo fuente de alimentación, observations, but their results are inconclusive concerning the participation II'Íaciones existentes en sus tubos digestivos. La of adults in larvae nutrition. Finally, Burnett et al, (1969) and Mason & 1 una estructura, que probablemente funciona corno Odum (1969) showed the importance of coprophagy in adults nutrition. ) de los adultos; dicha estructura no existe en las ~tos de la importancia que la xilofagia puede haber IOCial en estos insectos. Concerning the participation of symbiotic microorganisms iri the nutrition ofthese insects, Lewis (1926) and Pearse et al (1936) looked, unsuccesfully, ra, Comportamientos Parentales, Comportamiento for cellulotic protozoires in the gut of Odontotaenius disjunctus (Illiger). However, it is well known that bacterians and fungi are very. common in the intestines of Passalids, but it is unknown if they could have a significant participation in the nutrition of these insects (Lewis, 1926; Heymons & Heymons, 1934; Patterson, 1937; Lichtward 1957 & 1968; Baker, 1968). J

28 FOLIA ENTOMOL. MEX. 85 (1992)

V ALENZUELA: ALIMENTARY R In this P.aper 1 pr~ent results which show that Iarvae and young adults can~ot survive on a diet made exclusive! y of wood; furthermore, 1 illustrate In order to determine if Iarvae car the Importance of the ingestion of adult faeces for both larvae and adults. of wood, the following experiment wa punctiger Lepeletier et Servil METHODOLOGY ANO R.ESUL TS In the first (n= 18), the Iarvae were · (n= 19), larvae were also fed on woo In order to evaluate the preferences of larvae when allowed to choose of fine sawdust in order that the larv: between different kinds of food, the following selection tests were made: in of using this group was to determine i1 glass Petri dishes 10 cm in diameter, equal amounts of the materials being a feeding dependance on the adults, tested were placed, symmetrically, in both sides of said dishes · then one suggested by Ohaus (1900, 1909). 11 first instar. larvae of Passalus interstitialis Eschscholtz was put the c'enter ¡~ adult detritus. In order to avoid the t of ~ach dish. 24 hours later, the material which larvae were eating was placed individually in small plastic co registered. The results concerning longevity d ~ree ty~es of selection tests were made: a) between adult homospecitic on figure l. As no differences were o detntus (a mixture of wood and adult faeces) and fragmentated wood without in bits or in sawdust, the results of b< faeces (n = 27), b) between adult heterospecitic detritus and wood without heading (larvae fed on wood). As can fa~ces (n = 20) and, e) between homospecific adult and larva e detritus (a fed with wood survived over 8 days, ' mixture of wood and larvae faeces; n=20). adult detritus were still alive twenty None of the larvae of the first group at Tablc 1 13 Iarvae reached second instar, 7 the ~esults o~ thrcc diffcrcnt typcs uf sclcctiun tests maJe with larvae of P. punctiger [or J¡ffcrcnt kmds of fuod. The numbcr of larvae fccding in each suhstratum aftcr 24 hrs ¡8 rcprcscntcd. In the case of certain xylophagous due to the presence of symbioti Type of Fuod Num. of larvae x2 Wigglesworth 1976 and Chararas 1971 xylophagous cockroaches of genus Cr. Adult homospccitic detritus 23 13.4; p < 0.01 these microorganisms by means of the Wood detritus 4 which already have them. In order to Adult heterospccific detritus 18 12.8; p < 0.01 phenomenon in Passalids, the follo Wood detritus 2 punctiger Iarvae.

Adult homospccific detritus 16 7.2; p<0.01 A lot of29 newly boro larvae was 1 Larvae homocspccific detritus 4 feces) during 24 hours and later the) adult detritus used was mostly excrern Results are shown in tahle l. Significant differences were found in all was removed but, because of the smal cases. L~~vae always prefered to feed on adult detritus (horno or it was difficult to obtain a comp hetrospecihc) than on wood or larvae detritus. individually in small plastic container: J,

. )

OMOL. MEX. 85 {1992) ts which show that larvae and young adults VALENZUELA: ALIMENTARY RELATJONSHIPS IN PASSALIDAE 29 1tclusively of wood; furthermore, 1 illustrate of adult faeces for both Iarvae and adults. In order to determine if larvae can survive on a diet made exclusively of wood, the following experiment was carried out with first instar larvae of )LOGY ANO RESUL TS Passalus punctiger Lepeletier et Serville. Three groups of larvae were used. In the first (n= 18), the larvae were fed with bits of wood. In the second rerences of larvae when allowed to choose (n= 19), larvae were also fed on wood, but in this case it was in the form the following selection tests were made: in of fine sawdust in order that the larvae could better ingest it. The purpose lete~, equal amounts of the materials being of using this group was to determine if,in event that the larvae might exhibit Jy, m both sides of said dishes; then, one a feeding dependance on the adults, it could have a mechanical origen as erstitialis Eschscholtz was put in the center suggested by Ohaus (1900, 1909). The third group (n=35) was fed from le material which larvae were eating was adult detritus. In order to avoid the effect of cannibalism, the larvae were placed individually in small plastic containers covered with a fine mesh.

were made: a) between adult homospecitic The results concerning longevity during the first twenty days are shown ~ult faeces) and fragmentated wood without on figure l. As no differences were observed between larvae fed on wood, i heterospecific detritus and wood without in bits or in sawdust, the results of both groups were assembled under one homospecific adult and larvae detritus (a heading (larvae fed on wood). As can be seen in figure 1, non e of the larvae ~s; n=20). fed with wood survived over 8 days, while over 40% of those nourished on adult detritus were still alive twenty days after the beginning of the test. Tablc 1 None of the larvae of the first group attained the second instar; in the second ~tion tests madc with larvae of P. punctiger for 13 larvae reached second instar, 7 the third and 5 pupated. i larvac fceding in each substratum after 24 hrs is eprcscntcd. In the case of certain xylophagous insects, digestion of wood is possible due to the presence of symbiotic microorganisms (Hungate 1975, Num. of larvac x2 Wigglesworth 1976 and Chararas 1979). In sorne ofthem, like termites and 23 13.4; p < 0.01 xylophagous cockroaches of genus Cryptocercus, young individuals acquire 4 these microorganisms by means of the ingestion of feces from the individuals which already have them. In order to investigate the possibility of a similar 18 12.8; p<0.01 phenomenon in Passalids, the following test was carried out with P. 2 punctiger larvae.

16 7.2; p<0.01 4 A lot of29 newly born larvae was fed adult detritus (containing abundant feces) during 24 houJ:"s and later they were supplied only with wood. The adult detritus used was mostly excrement. Most of the wood contairied in it ~igniticant ditferences were found in all was removed but, because of the small size of sorne of the wood particles, : to feed on adult detritus (horno or it was difficult to obtain a complete separation. Larvae were kept wae detritus. 1 individually in small plastic containers covered with fine mesh. J

' ¡

30 FOLIA ENTOMOL. MEX. 85 (1992)

100 V ALENZUELA: ALIMENTARY

80 % OF SURVIVORSHIP OOK~~~------CL I (J) 60 o0: > 80 0:> \ :::J 40 (J) 1 60 * 1 20 1 40 1 1 o o 2 4 6 8 10 12 14 16 18 20 \ DAYS 20 \ \ ---- WOOD .... -+-- ADULT DETRITUS -----t- ADULT DETRITUS-W o o 20 40 60 80 Fig. l. Survivorship (in%), during the fll'St twenty days, of new-bom larvae fed with: a) wood (n=37), b) adult detritus (mainly fecal pellets) (n=35) and e) adult detritus for the first 24 hrs and then with wood (n=29). WOOD Results concerning the longevity of these larvae are also shown in figure l. As can be observed, the longevity was slightly greater than in the case of Iarvae fed exclusively with wood; however, al! individuals died befare Fig. 2. Survivorship (in %) of adults fed f[( attaining the age of 15 days. On the other hand, none of the larvae reached detritu.s (mainly fecal pellets) for the first 72 the second instar. These results prove that after a temporary but abundant ingestion of adult excrement, the larvae are still incapable of using wood as 20 individual pupae of P. pun their only source of food. resulting adults were fed exclusi· emergence. With another 20 pupae 2 With regard to adults, the insects collected in the field were able to this case adults obtained were fed survive for severa) months, under laboratory conditions, having wood as during the first 3 days and after the: their only nourishment. However, it is known that actually they need to reingest their own excrement for feeding (Masan and Odum, 1969), but they With adults, a longer time of feec al so need a constant supply of wood for the production of excrement suitable case of larvae, the latter being very · for feeding. In the absence of wood, adults die after sorne time, even if they are are not very active and apparent are able to reingest their feces (personal observations not published). In after emergence. For this reason, i arder to explore the possibility of a transmission of symbionts by excrements period of 72 hours in arder to guara in the case of adults, the following experiment was carried out: supplied. The results concerning the figure 3. MOL. MEX. 85 (1992)

VALENZUELA: ALIMENTARY RELATIONSHIPS IN PASSALIDAE 31

% OF SURVIVORSHIP OOK-=~=-----~------

80 \ 1 60 1 1 ,40 1 1 1 10 12 14 16 18 20 \ DAYS 20 \ \ ULT DETRITUS -- ADULT DETRJTUS-W o o 20 40 60 80 100 120 140 160 180 lwenty days, of new-bom llliVae fed with: a) wood DAYS ~) (n=35) ande) adult detritus for the first 24 hrs

WOOD - ADUL T DETRITUS+ WOOD ~ of thes~ larvae are al so shown in figure ty was slJghtly greater than in the case of 1; however, all individuals died befare Fig. 2. Survivorship (in %) of adults fed from cmcrgence with wood (n=20) and with adult e other hand, none of the larvae reached detritus (mainly fecal pellets) for the first 72 hrs and then with wood (n=20). ove that after a temporary but abundant 20 individual pupae of P. punctiger were put .on Petri dishes. The n-ae are still incapable of using wood as resulting adults were fed exclusively with wood from the moment of emergence. With another 20 pupae a similar procedure was followed but in ' th1s. case adults obtained were fed adult detritus plentiful in excrements ~cts collected in the field were able to during the first 3 days and after they were fed. only wood. !a~oratory conditions, having wood as . ~~ IS known that actually they need to With adults, a longer time of feeding on excrements was used than in the idmg (Mason an_d Odum, 1969), but they case of larvae, the latter being very voracious froms birth, while the former for the productwn of excrement suitable are are not very active and apparently start feeding a certain period of time ~ adults die after sorne time, even if they after emergence. For this reason, it was considered necessary to allow a rrson~ o_bservations not published). In period of 72 hours in order to guarantee a good ingestion of the excrements ransmJSSJOn Of symbionts by excrements supplied. The results concerning the longevity of these insects are shown in ~xperiment was carried out: figure 3. 30 FOLIA ENTOMOL. MEX. 85 (1992) V ALENZUELA: ALUv 100

OF SURVIVORSHIP 80 % 100·~=------

0.. I \ [f) 60 o0: 80 \ > > \ 0: 1 ::J 40 [f) ;ft 60 1 1 20 40 1 o 1 o 2 4 6 8 10 12 14 16 18 20 20 \ DAYS \ \ ---.-- WO O D --+- ADULT DETRITUS -- ADULT DETRITUS-W o o 20 40 60 Fig. l. Survivorship (in %), during the flfSt twenty days, of new-bom larvae fed with: a) wood (n=37), b) adult detritus (mainly fecal pellets) (n=35) and e) adult detritus for the first 24 hrs and then with wood (n=29).

Results concerning the Iongevity of these larvae are also shown in figure l. As can be observed, the longevity was slightly greater than in the case of Fig. 2. Survivorship (in %) of adl Iarvae fed exclusively with wood; however, al! individuals died before detritus (mainly fecal pellets) for ti attaining the age of 15 days. On the other hand, none of the Iarvae reached the second instar. These results pro ve that after a temporary but abundant 20 individual pupae of ingestion of adult excrement, the larvae are still incapable of using wood as resulting adults were fed their only source of food. emergence. With another 2C this case adults obtained 1 With regard to adults, the insects collected in the field were able to during the first 3 days and l survive for severa! months, under laboratory conditions, having wood as their only nourishment. However, it is known that actually they need to With adults, a longer tim reingest their own excrement for feeding (Masan and Odum, 1969), but they case of larvae, the latter bei1 also need a constant supply ofwood for the production of excrement suitable are are not very active and : for feeding. In the absence of wood, adults die after sorne time, even if they after emergence. For this r are able to reingest their feces (personal observations not published). In period of 72 hours in order · order to explore the possibility of a transmission of symbionts by excrements supplied. The results concer in the case of adults, the following experiment was carried out: figure 3. VALENZUELA: ALIMENTARY RELATIONSHIPS IN PASSALIDAE 31

% OF SURVIVORSHIP 100·~~------~------,

80 \ \ 60 \ \ 40 \ \ 20 \ \ \ --'J!E- ADUL T DETRITUS-W o o 20 40 60 80 100 120 140 160 180 DO'III~-bO,m larvae fed with: a) wood DAYS adult detritus for the fllSt 24 hrs WOOD - ADULT DETRITUS+WOOD are also shown in figure greater than in the case of 1 Fig. 2. Su¡vivorship (in %) of adults fed from cmcrgence with wood (n=20) and with adult individuals died before detritus (mainly fecal pellets) for the first 72 hrs and then with wood (n=20). none of the larvae reached a temporary but abundant 20 individual pupae of P. punctiger were put. on Petri dishes. The incapable of using wood as resulting adults were fed exclusively with wood from the moment of emergence. With another 20 pupae a similar procedure was followed, but in this case adults obtained were fed adult detritus plentiful in excrements during the tirst 3 days and after they were fed only wood. itions, having wood as that actually they need to With adults, a Ionger time of feeding on excrements was used than in the and Odum, 1969), but they case of Iarvae, the latter being very voracious froms birth, while the former .uc~Uo1n of excrement suitable are are not very active and apparently start feeding a certain period of time sorne time, even if they after emergence. For this reason, it was considered necessary to allow a not published). In period of 72 hours in order to guarantee a good ingestion of the excrements of symbionts by excrements supplied. The results concerning the longevity of these insects are shown in carried out: figure 3. 32 FOLIA ENTOMOL. MEX. 85 (1992) V ALENZUELA: ALil

Longevity of adults fed on wood from emergence varied from 9 to 36 days. In the case ofthose fed initially with excrement and subsequently with 80 wood, when the test ended, 150 days after it had begun, 8 insects were still ~ alive (40% of the total number). The results prove that newly emerged 60 adults are unable to survive exclusively on a wood diet. After ingesting 1-z UJ 1- excrements from older adults, however they are capable of using wood for z 40 o feeding. These results suggest the existence of a symbiont transmission ü z phenomenon which allows adult Passalids to take advantage of wood as their UJ 20 (9 main source of nourishment. o a: t: o Although from a nutritional point of view, the most remarkable z ~ adaptations of xylophagous insects are mainly related to the digestion of z o -20 structural polysacharides, consumption of nitrogen products also causes ¡::: < problems, due to their low content in wood (see for example: Chapman 0: -40 1975, Hungate 1975, Schmidt-Nielsen 1976, Chararas 1979). It was ~ therefore interesting to effect a comparative analysis of nitrogen content in -60 the wood consumed by Passalids as well as in their feces, considering the importance of coprophagy in these insects. I•LARVA For this purpose, third instar larvae of P. punctiger and adults were placed individually in Petri dishes. The insects were fed on wood for a week, and afterwards the nests were cleaned in order to eliminate excrement Fig. 3. Variation in nitrogen con relation to rotten wood on which t produced from the digestion of food consumed after the experiment. Later, as O in the figure, was of 0.09 %. insects continued to be fed with the same wood. These resúlts indicate th; Excrement produced in each nest was collected daily and kept in concentration than ingested refrigeration (at -5°C), as was a sample of the wood employed as food. The larvae, but less frequently. 1 Kjieldhal method was used to determine nitrogen content. To measure considerably less than those moisture content, 1 g of each sample was placed in an oven at 100°C for 24 hours and weighted immediatly after.

In figure 3, the percentage of increase or decrease of nitrogen in larvae In regard to feeding, xyl and adults faeces with respect to the originally ingested wood is represented. feeding on wood (see revisi~ For adults, in seven of ten repetitions, the nitro gen concentration increased Chararas 1979). On one h from 5.8 to 72.6%; in only three cases a decrease occurred (-1 to -27.7%). assimilable glucosides lik~ In larvae, in four cases an increase was noted (3.4 to 17.6% ), and in six glucosides disappear a rela1 other instances a decrease was registered ( -8.3 to -52.5%) and in one case consequentl y, these insects t no variation was observed. stage of decay. 85 (1992) V ALENZUELA: ALIMENTARY RELATIONSHIPS IN PASSALIDAE 33

11ergence varied from 9 to 36 :rement and subsequently with 80 lad begun, 8 insects were still ts prove that newly emerged ~ 60 a wood diet. After ingesting 1-z w 1- are capable of using wood for z 40 o ' of a symbiont transmission o z ~e advantage of wood as their w 20 (!} o a: 1- o ¡view, the most remarkable z ~ IY related to the digestion of z o -20 ~trogen products also causes ¡:: <( 1 (see for example: Chapman ii -40 6, Chararas 1979). It was :;; alysis of nitrogen content in -60 their feces, considering the

~- LARVAE FAECES CJ ADULT FAECE~ . punctiger and adults were ts were fed on wood for a order to eliminate excrement Fig. 3. Variation in nitrogen content (%) of fecal pellets produced by adults and lwvae in relation to rotten wood on which were fed. The nitrogen content of wood, represented after the experiment. Later, as O in the figure, was of 0.09 %.

These results indicate that adult excrement usually has a higher nitrogen ollected daily and kept in concentration than ingested wood. This phenomenon may also take place in wood employed as food. The Iarvae, but less frequently. Besides, increases registered in larvae tend to be rogen content. To measure considerably less than those registered in adults. in an oven at 100°C for 24 DISCUSSION

ecrease of nitrogen in larvae In regard to feeding, xylophagous insects present two different ways of ngested wood is represented. feeding on wood (see revisions by Chapman 1975, Wigglesworth 1976 and ogen concentrátion increased Chararas 1979). On one hand, there aré those able to use only easily e occurred (-1 to -27.7%). assimilable glucosides like saccharose, glucose and fructose. These (3.4 to 17.6%), and in six glucosides disappear a relatively short time after the felling of the trees; to -52.5%) and in one case consequently, these insects tend to feed on wood that is not in an advanced stage of decay. 34 FOLIA ENTOMOL. MEX. 85 (1992) V ALENZUELA: Al

On the other hand, there are those insects that can use structural symbionts) on food parü polysacharids from wall cells (like cellulose and hemicellulose) abundantly found in wood but which are more difficult to digest. Passalids dwell in However the most rer rotting wood which is in an intermediate stage of decay (Pearse et. al. 1936, In adults, in its upper se Gray 1946, Reyes-Castillo 1970, Schuster 1975, Valenzuela-González caeca. This condition de 1986a); this suggests that they could belong to the second group. Most temporary retention of f{)l insects able to feed on these polysaccharides (especially cellulose) depend on intestinal t1ora, could bt symbiotic microorganisms for feeding (Hungate 1975, Wigglesworth 1976, fundamental role in the Martin 1983, Terra 1990). insects (Chapman 1975

,i;· fermentation chamber, The results obtained show that larvae of Passalids are unable to feed dependance on adults. directly from wood. Newly emerged adults are also unable to use wood as their source of food unless they can ingest excrement from other adults first. However adults also Consequently, young adults are dependent on older adults for feeding, they also require the co although this dependence is only temporary. mentioned. This phenom1 food takes place at the pr Pearse et al 1936, working with O. dbjunctus found that adults can live to solve this problem wo on an a diet composed exclusively of wood, even if it had been sterilized. of food that has airead However, they did not experiment with newly emerged adults. chewing and intestinal t multiplication of microor The fact that recently emerged adults can only use wood for feeding after val ue. the ingestion of excrement from older adults, suggests the existence of a symbiotic relationship between passalids and microorganisms for the Mason's results (1966 degradation and/or assimilation of wood. Larvae, however, are notable to suggest that this is the cru feed directly on wood, even after the ingestion of excrement from older higher nitrogen content th adults. to Larroche and Grimaud and Odum ( 1969) ha ve su; This difference between larvae and adults as to. their ability to use wood function Ji ke an "extern: for feeding, is probably due to the variations in the structure of their during intestinal transit e digestive tracts (for sorne descriptions see: Lewis, 1926; Patterson, 1937; fecal pellets. Pereira & Kloss, 1966; Baker, 1968). In adults the digestive tract is longer in proportion to the body length than in larvae. In addition, in the case of In the digestive tract ol adults the digestive tract is rolled at severa! levels, a condition that does not symbiotic bacteria takes occur in larvae, which exhibit a more or less straight digestive tract. This French et al, 1976; Bentl feature could be an important factor in the digestion of wood. One of the of process occurs. Howev charasteristics of xylophagous insects, especially those able to feed on also be due to phenomena cellulose, is the great length of the digestive tract in comparison to that of to explore in the future. other insects. This fact allows for the prolonged action of enzymes (or (

85 (1992) VALENZUELA: ALIMENTARY RELATIONSHIPS IN PASSALIDAE 35

sects that can use structural symbionts) on food particles during transit (Chararas 1979). and hemicellulose) abundantly : to digest. Passalids dwell in However the most remarkable difference is observed at the proctodeum. 'of decay (Pearse et. al. 1936, In adults, in its upper section, there is an expansion formed by 6 rows of ~ 1975, Valenzuela-González caeca. This condition does not occur in larvae. Such a structure, where a g to the second group. Most temporary retention of tood particles occurs and which harbors an important ~pecially cellulose) depend on intestinal tlora, could be a fermentation chamber. Said chambers play a •te 1975, Wigglesworth 1976, fundamental role in the digestion of cellulose in sorne other xylophagous insects (Chapman 1975, Wigglesworth 1976). If this structure is a fermentation chamber, its absence in larvae could explain their feeding 1 Passalids are unable to feed 1 dependance on adults. re also unable to use wood as [ement from other adults first. However adults also depend on coprophagy for their feeding, although ¡on older adults for feeding, they also require the constant availability of wood, as has already been mentioned. This phenomenon could be due to the fact that the degrading of food takes place at the proctudeum, where absurption is mínima!. One way tus found that adults can live to sulve this problem would be with copruphagy, which allows reingestion ven if it had been sterilized. of fuod that has already been submitted to microbial action. Besides, emerged adults. chewing and intestinal transit uf the wood could favor acquisition and multiplicatiun uf microorganisms in feces, which could improve nourshing ly use wood for feeding after value. , suggests the existence of a d microorganisms for the Mason's results (1966, quoted by Mason and Odum 1969) and our own ae, however, are notable to suggest that this is the case. In fact, faeces have a greater caloric value and ·on of excrement from older higher nitrogen content than the wood from which they are made. According to Larroche and Grimaud ( 1988), this is al so true tor phosphorous. Mason and Odum (1969) have suggested that galleries where these insects live could to their ability to use wood function like an "externa! rumen" where transformation uf fuod, begun ns in the structure of their during intestinal transit continues, improving the nutritional quality uf the wis, 1926; Patterson, 1937; fecal pellets. the digestive tract is longer e. In addition, in the case of In the digestive tract of termites, phenomena of nitrogen fixation through els, a condition that does not symbiotic bacteria takes place (Benemann, 1973; Breznak et al, 1973; straight digestive tract. This French et al, 1976; Bentley, 1984). In Passalid it is not known if this type gestion of wood. One of the of process occurs. However, the increase of ~itrogen content in feces could ially those able to feed on also be dueto phenomena of this type, a possibility that would be worthwile ract in comparison to that of to explore in the future. nged action of enzymes (or 36 FOLIA ENTOMOL. MEX. 85 (1992) V ALENZUELA: ALit-. Wood is a plentiful resource in some habitats. In addition to supplying food for the insects dwelling in it, it can provide refuge against predators GRAY, l. E. 1946. Observations e and a relatively protected place against environmental fluctuations. 35: 728-746. HEYMONS, R. 1929. Uberdie biolc HEYMONS R, UNO H. HEYMONS. Nevertheless, its use as food has some restrictions due to its hardness, 40-51. low nitrogen content and difficulty in degrading and assimilating some of its HUNGATE, R. E. 1975. La celulos more abundant components like cellulose. For this reason, its use requires ]ARMAN, M. & P. REYES-CASTIU especial adaptations that frequently imply a symbiotic relationship. family groups. Acta Zool. MeJ LARROCHE, D. ANO M. GRIMAUO. de la teneur en phosphore du t As has been pointed out by Tallamy and Wood (1986), subsociality can alimentaire par des passalides. reduce the physical and nutritionallimitations of woody resources in severa! LEWIS, H. C. 1926. The alimenta ways. In Passalids, the adoption of wood as a nesting place and source of LICH1WARDT, K. E. 1957. Entm food has probably been one of the main factors in the development of the 463-474. LITCH1WARDT, K. E, 1968. Why • parental behaviors and, consequently, in the evolution of sociality in these MARTIN, M. M. 1983. Cellu1ose d insects. MASON, W. H. ANO E. P. Q[ bioelimination of radionuclide AcKNOWLEDGEMENTS Radioecol. (Michigan): 721-72 Mlll.ER, W. C. 1931. Sorne observ We are grateful to: M. L. Castillo, G. Halffter, C. Huerta and P. Reyes­ Ac. Se. 31: 266. M!ll.ER, W. C. 1932. The pl Castillo for their critica! reviews of the manuscript. We are indebted to M. (Lamellicomia). Ann. Ent. Soc Pérez, and A. L6pez for able technical assistaoce. We also wish to thank A. ÜHAUS, F. 1900. Bericht uber eine Valenzuela and l. Márquez for his help with the English version of the Zeit. 61: 164-173. manuscript. OHAUS, F. 1909. Bericht uber eine Zeit. 70: 1-39. PATTERSON, M. T. 1937. The cel REFERENCES comutus F. Ann. Ent. Soc. Am PEARSE, A. S., M. T. PATTERSON, BAKER, W. V. 1968. Thc gross slructure and histology ofthc udult und larval gut uf Pentalobus Passalus comutus Fabr., a bee barbatus (Colcoplcm: Pussalidac). Caruulian Entom. ]()(): 1080-1090. PEREJRA, F. S. ET C. M. KLOSS BENEMAN)II, J. R. 1973. Nitrogcn tixntion in tcnnitcs. Science Wash. 181: 164-165. Passalidae (Col.) americanos. J BENTU:Y, B. L. 1984. Nitro gen tixatinn in h:nnitcs: fate of ncwly tixcd nitrngcn. J. lnsect REYES-CASTIUO, P. 1970. Coleop Physiol. 30:653-655. géneros americanos. Folia En/( BREZNAK, J. A., W. J. BRilL, J. W. MEKDNS AND H. C. Cüi'I'EL. 1973. Nitrogcn fixation in REYES-CASTIUO P. & M. ]ARMA1 tennitcs. 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ObseJVations on teh life history of the homed Passalus. Amer. Midl. Nat. rnmental fluctuations. 35: 728-746. HEYMONS, R. 1929. Uber die biologie der Passalus kafer. Z. Morph. Oekol. 1iere. 16: 74-100. HEYMONS R, UNO H. HEYMONS. 1934. Passa/us und seine intestinale flora. Biol. Zentr. 54: ltrictions due to its hardness, 40-51. 1g and assimilating sorne of its HUNGATE, R. E. 1975. La celulosa en la nutrición . C.E.C.S.A., México. 36p. r this reason, its use requires ]ARMAN, M. & P. REYES-CASTillO. 1985. Mandibular force of adult and IUJVal Passalidae in rmbiotic relationship. family groups. Acta Zool. Mex. 12:13-22. LARROCHE, D. ANO M. aruMAUO. 1988. Recherches sur les Passalides africains. III. Evolution de la teneur en phosphorc du bois en decomposition suite a son utilisation comme substrat Vood (1986), subsociality can alimentaire par des passalides. Acles Coll. lnsecles Sociaux, 4: 103-110. of woody resources in several LEWIS, H. C. 1926. The alimentary canal of Passalus. Ohio Joumal Sci. 26: 11-24. • nesting place and source of LICHTWARDT, K. E. 1957. Enterobryus atlenuatus from the passalid . Mycologia. 49: 463-474. ~rs in the development of the LITCHTWARDT, K. E, 1968. Why stop with the . Turtox News. 46: 194-196. evolution of sociality in these MARTIN, M. M. 1983. Cellulose digestion in insects. Comp. Biochem. Physiol. 75:313-324. MASON, W. H. ANO E. P. OOUM. 1969. The effect of coprophagy on retention and bioelimination of radionuclides by detritus-feeding animals. Proc. Second Nat. Symp. ns Radioecol. (Michigan): 721-724. Mlll.ER, W. C. 1931. Some observations on the habits of Passalus comutus (Coleoptera). Ohio Ac. Se. 31: 266. ~er, C. Huerta and P. Reyes­ Mlll.ER, W. C. 1932. The pupa-case building activities of Passalus comulus Fab. ~cript. We are indebted to M. (Lamellicomia). Ann. Enl. Soc. Amer. 25: 709-712. ~ce. We also wish to thank A. ÜHAUS, F. 1900. Bericht uber eine entomologischz reise nach Central Brasilien. Slelt. 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TAUAMY, D. W. & T. W. WOOD. 1986. Convergence pattems in subsocial .B. Ann. Rev. (COLEOPTERA: :MEI Enromol. 31: 369-390. TERRA, W. R. 1990. Evolution of digestive systems of insect.B. Ann. Rev. Entorno/. 35:181-200. V ALENZUElA-GoNZALEZ, J. 1986a. Life cycle of the subsocial bectle Heliscus lropicus in a tropical locality in southem Mex.ico. Folia Enromo/. Mex. 68:41-51. VALENZUElA-GoNZALEZ, J. 1986b. Territorial behavior of the subsocial bectle Heliscus lropicus under laboratory conditions (Coleoptera, Passulidae). Folia EnlotruJl. Mex. 70:53- 63. VALENZUElA-GoNZAl.F.Z, J. Y M. L. CAS11ll..O. 1984. El comportamiento de cortejo y cópula en Heliscus lropicus (Coleoptera, Passalidae). Folia Enlotnol. Mex. 61:73-92. WIGGLESWORTH, V. B. 1976. lnsect physiology. M~!!huen, London.

Folia Entomológica Mexicam

1 Investigador de Carrera, colaboralli la Dirección Nacional de Promoción Argentina).

Recibido para publicación: 28 de ma Aceptado para publicación: 30 de ag