Biotic Decimating Factors Affecting the Distribution of ...

Muhammad & Ande: Biotic decimating factors affecting the distribution of Cirina forda population 57

West African Journal of Applied Ecology, vol. 22(2), 2014: 57–68.

Biotic Decimating Factors Affecting the Distribution ofCirina forda Westwood (Lepidoptera: Saturniidae)Population in Niger State, Nigeria

M. I. Muhammad1 and A. T. Ande2

1Department of Basic Sciences, College of Agriculture, P.M.B, 109, Mokwa, Niger State2 Department of Zoology, University of Ilorin, Kwara State, NigeriaCorresponding author; Email: [email protected]

AbstractThe biotic agents, i.e. predators, parasites and pathogens that could be responsible for the mysterious occurrenceand decimation of C. forda (Westwood) in Niger State, Nigeria, were monitored, identified, and their individualinteractive effects reported from farm lands and villages from six local government areas, namely Katcha,Paikoro, Gurara, Lavun, Lapai and Rafi. All the developmental stages, i.e. eggs, larva, pupa and adult of C. fordahad a biotic agent affecting them. The checklist of the agents include Anastatus spp, an egg parasitoid; larvalpredator including Ocecophyla longinoda; Spiders, and black crow bird; larval pathogens of viral origin, i.e.Nuclear polyhedrosis virus and Granulosis virus and of fungal origin i.e. Nomerae arileyi and Beauveriabassiana; a pupalparasitoid, Hockeria spp;and Agama lizard, a predator of imago stage. The possible roles ofeach of these agents in the ephemeral nature and beliefs about the mysterious distribution of C. forda weresubstantiated and discussed.

IntrodutionThe emperor moth, Cirina forda Westwood(Lepidoptera: Saturniidae) caterpillar, is oneof the most popular edible food insects inNigeria (Fasoranti & Ajiboye, 1983; Ande,1991; Ande & Fasoranti, 1995). Like all otherLepidopterans, C. forda is holometabolous(Ande & Fasoramti, 1996, 1997). It istypically an African moth whose sole host isthe shea butter tree, Vittelaria paradoxa(Ande,1991; Ande & Fasoranti, 1996). C.forda distribution coincides with theoccurrence of V. paradoxa in Nigeria withNiger State featuring very prominently(Ande, 1991). C. forda is a univoltine insectwhose caterpillar, i.e. the most conspicuousdevelopmental stage, are noticed betweenJune and September annually (Ande &Fsaoranti, 1997). The caterpillars defoliatematured fruiting-bearing trees, thus, causing

extensive damage to V. paradoxa trees(Greenwood, 1929) such that 90% of thetrees’ leafy area is damaged in a season(Owusu-Manu & Kuma, 1990).Unfortunately the period of this caterpillarattack coincides with the period of seedmaturation and ripening of V. paradoxa fruits(Ande & Fasoranti, 1995).

The occurrence and distribution of thisinsect remains a mystery as they are generallyregarded as ephemeral. Even locations thatare renowned for their presence, when theyare in season, frequently come up with noharvest or very low yield even in contiguousharvest seasons. Some of the factorsresponsible for this undesirable developmentinclude environmental factors such as bushburning and biotic decimating factors thatinclude human factors such as inordinateharvest pressure, over cropping and mode

West African Journal of Applied Ecology, vol. 22(2), 201458

of harvest (Ande, 1991). Other biotic factorssuch as predators, parasites and pathogensabound, but dearth of knowledge with respectto specific forms of these and their respectiveinteractive activities have been identified,more so that the quality and importance ofeach of these factors vary with location. Anattempt is made in this paper to report forthe first time the various decimating bioticfactors that affect the natural field populationof C. forda in Niger State, Nigeria.

Materials and methodsNatural field population of C. forda in sixlocal government areas, i.e. Katcha, Paikoro,Gurara, Lavun, Lapai and Rafi in Niger Statewere monitored for predatory, parasitic,pathogenic and other vertebrates over twoseasons. Farmlands and villages featuringthriving populations of C. forda wereidentified based on positive responses to thequestionnaires in 2009 and confirmatoryvisitations in December–April for pupae;June for adults; June–July for eggs and July–September for various instars of larvae inthe cropping season to the sites were utilisedfor the study in 2010 and 2011. Each of theselocations were frequently visited andscrutinised for biotic interactions that resultedin reduced viability or mortality of each ofthe developmental stages of C. forda on thefield. A three 10-m2 subloci were mappedout of each locus (100 m2) to providereplicate values per study site.

Soils around V. paradoxa plant base andwithin one meter quadrat were scrappedcarefully with a hoe and shovel (three randomthrows of quadrat per sublocus and, or ninethrows of quadrat per site. The total numberof pupae per site was taken in each localgovernment area. All pupae encountered werecarefully uprooted and mean density and

(SD±) noted. The living status of each wasascertained by rocking the abdomen and meandensity and (SD±) of survival pupae noted.Stiff abdomen indicated dead pupae while aresponsive pupa was living, the experimentfor pupal parasites and parasitoids was putunder observation daily for 5 days forpathogens and parasitoid emergence usingsterilised plastic containers with a layer offilter paper at the bottom.

The containers were placed in abiochemical incubator (ZSD-1160, Zhcheng,China) maintained at 25 ± 2 0C and 75–80% RH. Fungus infested individualscollected dead and those dying in thelaboratory were placed in microscope slideson moist filter papers in petri dish for 1 weekto stimulate sporulation of fungi. Anyemerging fungal pathogen was isolated byinoculating the conidia onto potato detroseagar (PDA) and fungal growth (Odebiyi etal., 2003) and the microbes identified wereconfirmed at the Microbiology Departmentof Federal University of Technology, Minna,while pupal parasitoids identified wereconfirmed at Insect Museum andIdentification Unit of Institute of AgriculturalResearch, Ahmadu Bello University, Zaria.

ResultsAll the developmental stages, i.e. egg, larva,pupa and adult, of C. forda were affectedby different biotic agents, Table 1ab.

EggsEggs of Cirina forda in Niger State were

conspicuously destroyed by a parasitoid waspidentified to be Anastatus spp. (Fig. 1a).The ovarian chalcid wasp is a minuteindividual 2–4 mm long, very active, briskand had wing patterns, which makes it lookedmore like small black ants with metallic black


TA

BL

E 1

aE

ffec

ts o

f bi

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age

nts’

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and

inte

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of C

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LGA

Mea

n (S

D±

) of

pup

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Mea

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(SD

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nfes

tati

on20

1020

1120

1020

1120

1020

1120

1020

1120

1020

11

Gur

ara

147.

14 ±

37.

448

.8 ±

7.0

818

±8.0

434

.07

± 16

.913

1.7

± 37

.824

.42

± 11

.293

.3 ±

16.

027

± 1

0.5

1.5

± 1

4.7

1.5

± 5

.1

Kat

cha

102

± 33

.372

82 ±

28.

618

32 ±

16.

294

33 ±

3.7

4970

± 2

8.38

168

± 1

5.87

461

.3 ±

24.

060

.± 1

3.7

1.5

± 1

4.7

2.0

± 1

4.7

Lap

ai42

± 5

2.26

344

.5 ±

50.

745

± 3

8.18

314

.6 ±

13.

4822

.6 ±

23.

0622

.8 ±

40.

2912

.4 ±

6.2

220

.± 1

7.5

1.8

± 1

4.0

1.0

± 5

.19

Lav

un77

.4 ±

42.

5077

.4 ±

41.

640

.5 ±

36.

3740

.8 ±

37.

6945

± 1

2.72

720

.2 ±

12.

2339

.5 ±

22.

339

± 1

9.3

1.0

± 1

2.7

1 ±

11.0

Paik

oro

60.3

± 1

7.51

44.7

± 1

7.7

24.7

± 7

.977

16 ±

8.7

4640

.5 ±

11.

4228

.8 ±

14.

5744

.3 ±

15.

638

± 1

5.9

1.5

± 3

.61.

7 ±

4.3

Raf

i42

± 1

3.74

729

.25

±13.

59.

0 ±

0.0

6.0

± 5

.196

36 ±

15.

588

14.7

± 1

4.77

26.6

± 1

2.8

20 ±

8.7

1 ±

5.1

961.

2 ±

4.5

TA

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and

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LGA

Egg

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age

(egg

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Bea

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(NP

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)(N

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Bb)

2010

2011

2010

2011

2010

2011

2010

2011

2010

2011

Tot

alIn

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Tota

lTo

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Tota

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tal

Tota

lTo

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Tota

l(%

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)(%

)(%

)(%

Gur

ara

587

480

(81.

7)72

360

8 (8

4)23

8 (7

5.5)

197

(62.

8)77

(24.

4)17

0 (7

5.3)

––

––

Kat

cha

827

471

(56.

9)91

977

1 (8

0)17

9 (4

4)18

0 (4

4.4)

46 (1

1.3)

45 (1

1.1)

119

(29.

3)10

4 (2

5.6)

61 (1

5.0)

75 (1

8.5)

Lap

ai44

236

9 (7

8.1)

535

438

(81)

200

(74.

0)14

4 (5

3.3)

70 (2

8.9)

124

(49.

6)–

––

–

Lav

un44

733

7 (7

5.3)

576

479

(81)

164

(72.

8)17

0 (7

5.3)

59 (2

6.2)

55 (2

4.4)

––

––

Paik

oro

816

568

(69.

9)95

081

4 (8

5)23

7 (5

2)23

7 (5

2.6)

213

(47.

3)21

3 (4

7.3)

––

––

Raf

i23

216

0 (6

8.9)

382

250

(82)

108

(60.

0)10

8 (6

0.0)

72 (4

0.0)

72 (4

0.0)

––

––


body. This wasp in the family of Chacididaewith an ovipositor protruding strongly usedthe ovipositor by the female Anastatus spp.to puncture the egg chorion, and usuallyfound roaming around the cluster of C. fordaegg mass. All the eggs destroyed byAnastatus spp. were empty shells (Fig. 1b).During the two sessions, over 66% in 2010and 82% in 2011 of egg masses examinedwere attacked by Anastatus across NigerState.

LarvaePredatory attack of C. forda larvae by the

adult red ants, Oecophyla sp. werefrequently noticed across the State and in allthe local government areas sampled. The 1and 11 instars were most affected. The antsattacked their prey by biting, demobilisingand retrieving them to their nests fordevouring. The mature C. forda instars werealso vulnerable, as the gregarious predatorsgathered to demobilize them from theirresidence constructed from leaves of V.paradoxa (Fig. 2) in the canopy of the hostplant.

The same was the case with the solitaryspiders, residing on the leaves and trunk ofthe V. paradoxa canopy. Three differenttypes of these spiders were recovered, oneof which was identified as Opisthoncuspolyphemus (Fig 3a).The other two wereidentified to be members of the familySalticidae and Thomisidae. These spidersbounced on their prey individually fromhiding or webbed them up, after which theybite and paralyzed the larvae before suckingthe juice out of their preys, leaving behindthe undigested exoskeletal excuvie (Fig.3b).The Blackcrow birds, Corvuscapensis,(Fig. 4abc) fed on all C. forda larval instarsby probing and picking them up from the

twigs of host trees across the State. Twofungal species, Nomeraearileya (Moniliales,family Moniliaceae), and Beauveria bassiana(Hypocreales: order Cordycipitaceae) wereisolated from C. forda larvae in Niger State.The hyphae of the fungus, Nomeraeaerileyi,(Moniliales: Moniliaceae) a dimorphichyphomycete, emerged on the larval cuticle atthe intersegmental membranes producedspores that was seen as creamy reddishbrown powder enveloping the body.

The fungus was responsible for epizooticdeath of C. forda larvae in all the sampledlocations that were damp across Niger State.The affected larvae were relatively inactiveand became stiff prior to death with anobservable coloured mould attachmentemerging from the intersegmental regionssoon after death (Fig. 5). Since the infestationof this fungus was not detectable at the onsetuntil after the larvae had stiffened out, it wasnot possible to determine spontaneousoccurrence or the infestation. Beauveriabassiana is an entomopathogenic fungus thatinfected the larvae of C. forda. They arecontact-pathogens that replicated on cuticularsurface of the larvae and developed a whitishmould that continued to increase even afterthe dead of the larvae (Fig. 8), or thedestructive capability of the pathogen perlocation. Dead larvae featuring this diseasewere, however, more frequent in KatchaLGA, seen sometimes in an upright positionstill attached to a leaf or stem in an upperpart of the trees.

Two virus types i.e. Nuclear polyhedrosisvirus(NPV) and Granulosisvirusis (GV)were encountered infesting C. forda larvaein Niger State. Nuclear polyhedrosis virus(NPV) is C. forda larvae pathogen most likelycontacted from ingesting virus-contaminatedfoliage. Once contacted, the larval feedingand movement capabilities were affected.


Fig. 1a. Anastatus spp. caught in the act of destroying the egg clusters.

Fig. 1b. The destroyed eggmass by the ovarian parasitoid, Anastatus spp.


Fig. 2. Ocecophyla longinoda in their nests on host tree where they retrieved their preys into.

Fig. 3a and 3b. Larvae were webbed massively to dead by spider and, the wilted larvae can be seen in silks ofspider.


Fig. 4a.Blackcrow on a twig resting after picking larvae of Cirina forda.

Fig. 4b. The Blackcrow captured on the field contagious with larval population of Cirina forda.


Fig. 5. Nomerae arileyi infested larva in cotton cream coverage in an inactive but stiffened position hanging onthe leaf in upper part of the tree

Fig. 6. NPV-infected larva becomes black and eventually dies hanging.


Fig. 7. GV-infected larva differs from NPV-infected by turning milky white and stops feeding.

Fig. 8. Beauveria bassiana-infected larva died hanging with white cuticular coverage that turned black later, thefungus enzyme showed the presence of beauvericin toxin.


The NPV-infected larvae became sluggishand stopped feeding, only to develop awhitish ventral region that turned black alongthe intersegmental membranes as skindarkens and eventually died hanging as shownin Fig. 6.

Granulosis virus infection was similar toNPV in most respect . GV infested larvaeturned milky white and the skin of the larvaebreaks easily to release the infectious virus(Fig. 7). The matured larval instars, i.e. 5thand penultimate instars, were devoured bythe Hedgehog, a spiny rat (Fig. 9) that werereadily observed within the ecosystem understudy, hence, they predated frequently onlarvae attempting to bore into the soil to formpre-pupa.

PupaeHockeria spp. (Walker), a Hymenopteran

chalcidparasitoid wasp species of thesuperfamily Chalcidoidae and suborder

Fig. 9a. Hedgehog. Feeds on the fifth and penultimate larva, (B) devoured larva preyed upon by hedgehog.

Apocrita, was the only biotic agent observedparasitizing on the pupae of C. forda in NigerState. Mature Hockeria spp. parasitoidemerged from pupal body by which time thepupa was dead. The parasitoid, Hockeriaspp, was usually active on bright and clearday and had a colour range of black tobrown with armoured and sclerotized body.They oviposited eggs on pupal body of theCirina forda using stout ovipositor. Theysubsequently developed within the pupae toadult wasp that emerged from the pupal case.The infected pupae took sometimes,approximately 46 days to die.

AdultAgama spp. predated on the imgo of C.

forda. This was, however, not frequentlyobserved, as the C. forda adults rooted onV. paradoxa tree canopy where the lizardsseldom occur during the day.


DiscussionWhereas the egg, pupa and adultdevelopmental stages of C. forda had onebiological agent each of the larval stage,which happens to be the most easily noticed,the most destructive to host plant and thesole stage responsible for its dispersal (Ande,1991) had the largest number of adversarialbiological agents. These agents includedpredators and pathogens. Although it was notpossible to determine the instantaneousdecimating effect and dispersal mode of thepathogens amongst the larvae, its cumulativeeffect may be colossal since the mature larvaeand pre-pupa stages are the stages consumedby humans and most of the time thesepathogens would have killed its host beforeit matures. Mermithid nematode infestation,reported to emerge from the body of maturelarva and pre-pupa (Ande, 1991), was neverobserved in this study. The possibility of asnake predating on pre-pupae descending thetree (Ande, 1991) may exist but was notobserved throughout the study period. Thesepredatory activities contributed significantlyto decimation, especially predation of theearly vulnerable instar stages by Oechophylaand the spiders.

The gregarious habit of C. forda at thelarval stage nullified the effect of decimationof this stage by these numerous agents, thus,their impact was hardly noticed.Unfortunately the larvae that matured to thefourth and fifth also fell victims of thepathogens and predators just as fungalpathogens such as Trichoderma sp .Aspergillus nigers, A. flavus and Fusariumsolani were implicated by Odebiyi et al.(2003). Thus, few larvae actuallytransformed successfully to pupae. Man infact can also be listed as a major C. fordalarval predator, since he often harvested the

larvae enmass for consumption and as anitem of commerce (Ande, 2002). The adultstage also featured a predatory agent, i.e.Agama spp. but the effect of this was notconspicuous as they did not share the sameecological niche. Apart from this, adult C.forda were only active at night ( 11:00 p.m.–5:00 a.m. ) for 2–3 days (Ande & Fasoranti,1997), during which the poikiothermicreptiles (Agama lizards) are inactive andresting. Unfortunately as predators, thereptiles have preference for active or mobileinsects within reach. Fortunately C. fordaadults do not qualify, as they are inactiveand situated high up on the host tree (Ande,1991).

The pathogens recorded included twoviruses, i.e. Nuclear polyhedrosis virus,Granulosis virus and two fungi, i.e. Nomeraearileya, and Beauveria bassiana both ofwhich contributed to the reduction inpopulation of C. forda larvae considerably,especially at the mature larva stage of fourthand fifth instar. The parasitoids wererestricted to the egg and pupa developmentalstages despite their seemingly hard protectivecovering. The pupalparasitoid, Hockeria spp.featured quite prominently in Niger State.Dwomoh et al. (2004) noticed a similarsituation in Ghana where pupae of C. fordashowed high presence of Hockeria spp.infestation, particularly pupae collected inDecember and January. The activity of thispupal parasitoid may be distinctly lessdestructive at 30.4% in 2010 and at 41% in2011, as compared to the egg parasitoid, asvirtually all eggs in a cluster (60% in 2010and over 82% in 2011) were infested asagainst individual pupal infestation. However,the dead percentage rate of pupae eventuallyrose with some dying in the laboratory.


ConclusionFor the first time, field experiment hasidentified the biotic decimating factors ofCirina forda in Niger State, Nigeria. Thesefindings proffered answers to the ephemeralnature and beliefs about the mysteriousoccurrence, dispersal and distribution ofCirina forda. The numerous insidious anddevastating activities of predators, parasitesand pathogen identified no doubt culminatedin the decline and distinction of Cirina fordapopulation. The study is ongoing on theimpact of each and collective depletingactivities on the distribution and populationof C. forda in Niger State, Nigeria.

AcknowledgementsThe authors are grateful to the HigherNational Diploma (HND) students of NigerState College of Agriculture, Mokwa, NigerState, Nigeria, for their technical assistance,and Local Government staff as farmers’contact of the six local government areas ofNiger State, Nigeria, for their assistance whenconducting the trial.

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Dwomoh E. A., Akrofi A. Y and Ahadzi S. K. (2004).Natural Enemies of the Shea defoliator, Cirinaforda, Tropical Science. 44: 124–127.

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