Research Article |
Corresponding author: Thea Lautenschläger ( thea.lautenschlaeger@tu-dresden.de ) Academic editor: Pavel Stoev
© 2017 Thea Lautenschläger, Christoph Neinhuis, Mawunu Monizi, José Lau Mandombe, Anke Förster, Thomas Henle, Matthias Nuss.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lautenschläger T, Neinhuis C, Monizi M, Mandombe JL, Förster A, Henle T, Nuss M (2017) Edible insects of Northern Angola. African Invertebrates 58(2): 55-82. https://doi.org/10.3897/afrinvertebr.58.21083
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From 2013–2017, we accompanied and interviewed local people harvesting edible insects in the Northern Angolan province of Uíge. Insect and host plant samples were collected for species identification and nutritive analyses. Additionally, live caterpillars were taken to feed and keep until pupation and eclosion of the imago, necessary for morphological species identification. Altogether, 18 insect species eaten by humans were recorded. Twenty four edible insect species were formerly known from the country, four of which are confirmed in this study and 14 species additionally recorded. Sciatta inconcisa Walker, 1869 (Erebidae) and Gastroplakaeis rubroanalis Wichgraf, 1913 (Lasiocampidae) are reported for the very first time as human dietary foods. All 18 species are illustrated and DNA-Barcodes are provided to enable re-identification of species. Though much effort has been undertaken for the identification of the 18 species, only 14 species have been identified at species level and another four only at family level. The scientific names are listed along with the vernacular names. A nutritional analysis is provided for nine species most of which are consumed in the villages, but some are also traded, for which a market study has been conducted. Information is also given on traditional collection and preparation as well as cultural aspects of edible insects in Northern Angola.
Edible insects, DNA-barcoding, nutritional values, market study, Uíge province
The consumption of insects by humans is commonly found in the Americas, Africa, Asia and Australia (
The number of insect species consumed by people in Africa ranges from 250 (
However, until the present time, only 24 species of edible insects have been recorded from Angola, 19 of which are identified at species and five at genus level. These records are scattered over publications from a period of more than a hundred years (
Scientific research on this topic is scarce for Angola even though there is reason to presume that consumption is comparably common in adjacent countries. Much more data has been compiled from regions adjacent to northern Angola.
Due to the available data from adjacent regions, it is to be expected that many more insect species are eaten by humans in Northern Angola than previously recorded in scientific literature. Decades of war have hindered the exploration of this area. The most compelling argument in favour of insects as food is their nutritional value, especially since they are rich in protein, vitamins and minerals, iron and B-vitamins (
In the following, we present the data for a first survey of the consumption and trading of edible insects in Northern Angola and provide information on their nutritive, as well as their commercial, values.
Our survey was conducted in the Province Uíge between 6 and 8 degrees latitude south and 14 and 17 degrees longitude, bordered to the north and east by the Democratic Republic of Congo, to the south by the provinces of Malanje, Cuanza Norte and Bengo and to the west by the province of Zaire (Fig.
Large areas are heavily disturbed anthropogenically and elements of Zambezian flora have greatly increased in abundance following destruction of the original vegetation leaving secondary grass- and woodland (
The province Uíge comprises 16 municipalities, covering an area of 58,698 km2 housing over 1.4 million inhabitants (
Field surveys in Uíge Province were performed during six trips in November 2013, January-February 2014 and February 2015, July 2015, November 2016 and February 2017. One trip to the Calandula falls in Malanje Province completed the survey in February 2017.
Edible insects were sampled in collaboration with people from the villages in order to learn where and when to find the insects that are used as human food. Along with the sampling, semi-constructed interviews with local collectors took place to detect larvae as well as their host plants, the local Kikongo names, preparation and possibly even its commercialisation. Seventeen villages in eight different municipalities Uíge, Puri, Mucaba, Bungo, Negage, Damba, Kangola and Quimbele, were therefore visited to collect larvae from forest and savannah.
Since most of the edible insects are moth larvae and taxonomy of the moths is mainly based on imagoes, larvae were taken alive and fed with their natural plants until pupation. Pupae were placed in an incubator until eclosion of the imagoes. Additionally, moths were attracted by artificial light to analyse the phenology of the species and to enable molecular identification of larvae by comparison with the imagoes.
One part of each sample was stored in absolute ethanol for later morphological and molecular identification while the other part was deep frozen for nutritional analyses. Moths were killed with cyanide and quickly dried in paper envelopes for later morphological and molecular identification. Voucher specimens are preserved at the Senckenberg Museum of Zoology Dresden on behalf of TU Dresden due to its having appropriate facilities.
Plants were photographed and voucher specimens collected, dried and stored at the Herbarium Dresdense, Technische Universität Dresden, Germany.
In a Memorandum of Understanding between the Instituto Nacional da Biodiversidade e Áreas de Conservação (INBAC), Angola and the Technische Universität Dresden, Germany, signed in 2014, it was agreed that, as soon as appropriate conditions to store the insect and herbarium vouchers had been established, duplicates would be returned to Angola. Collection and export permits were issued by the Ministry of Environment Angola and the Province Government of Uíge. Identification of reported plant specimens and data analyses were completed in Dresden, Germany.
Insects were identified based on morphological characters and by using traditional taxonomic literature as well as based on the DNA-Barcode.
For morphological identification, moths were placed in a relaxing jar and wings spread on a spreading board. After labelling, they were identified based on wing pattern elements using taxonomic literature (
The material for DNA isolation is derived from either canned (99% absolute) caterpillars or from dried moths. For the extraction, tissue from the abdomen (caterpillars) or a leg (imagoes) was used for this purpose. The DNA was extracted with the NucleoSpin Tissue Kit (Macherey-Nagel) according to the manufacturer’s protocol.
The mitochondrial COI gene was amplified using the primers HybLCO (forward) and HybHCO (reverse) (
Standard PCRs were performed in a total volume of 20 μl using 1.5 µl of DNA of concentration as extracted, 0.5 unit Bio-X-ACT short DNA polymerase (Bioline) in the recommended buffer, 2.5 mM of each dNTP (Fermentas), 0.25 µM of forward and reverse primer and 2.5 mM MgCl2 (Bioline).
Cycling conditions were as follows: 39 cycles were used with denaturation at 94 °C (30 s but 5 min for the first cycle), annealing at 49 °C (30 s) and extension at 72 °C (45 s but 10 min for the last cycle).
PCR results were examined via gel electrophoresis on a 1% agarose gel and GelRed as dying agent. Successful PCR samples were cleaned with ExoSAP-IT™ [Exonuclease I (Exo) and Shrimp Alkaline Phosphatase (SAP)]. PCR and ExoSAP-IT™ were performed on an Eppendorf Mastercycler S thermo cycler. For the Sanger-sequencing PCR reactions, we used 0.25–3.0 μl PCR sample, depending on the thickness of the respective agarose gel band and 160 nM of the sequencing primers T7 (forward) or T3 (reverse), 0.5 μl BigDye, 2.25 μl BigDye-sequencing buffer and made up with distilled water to the 10 μl reaction volume. Sequencing was conducted either at the Senckenberg Museum of Zoology Dresden (ABI 3730 Genetic Analyser; Applied Biosystems) or at Macrogen Europe. Sequences were aligned using Bioedit version 7.2.5. and analysed in MEGA 7.025 using the Neighbour Joining Algorithm. Sequences were submitted to GenBank (see Table
Species overview. Scientific and vernacular names of insects and host plants according to local Kikongo dialect, except one name, which is marked with (Kim.) according to Kimbundu language; Plant names according to plantlist.org; plant family in square brackets; [ARE] Arecaceae, [CAN] Cannabaceae, [EUP] Euphorbiaceae, [FAB] Fabaceae, [MOR] Moraceae, [MYRI] Myristicaceae, [MYRT] Myrtaceae, [PHY] Phyllanthaceae, [SAP] Sapindaceae, [STE] Sterculiaceae; voucher number of herbarium sheets according to Herbarium Dresdense, vouchers marked with F are photo vouchers.
Insect species | Vernacular insect name | ID | NCBI | Host plant species | Vernacular plant name | Vouch. no. |
---|---|---|---|---|---|---|
LEPIDOPTERA Saturniidae | ||||||
Cirina forda (Westwood, 1849) | Nkuati | R24 | MG489854 | Erythrophleum africanum (Benth.) Harms) [FAB] | Ngungu | 43233 |
Nkuati | Burkea africana Hook. [FAB] | Kilobo | 44200 | |||
Imbrasia epimethea (Drury, 1772) | Monguela | R20 | MG489850 | Celtis gomphophylla Baker [CAN] | Pau capitão | 44219 |
Monguela | R23 | MG489853 | Ricinodendron heudelotii subsp. africanum (Müll. rg.) J.Léonard [EUP] | Monguela | 42845 | |
Nsati | R15 | MG489845 | Vukua | 45866 | ||
Monguela | R21 | MG489851 | Ricinodendron heudelotii subsp. africanum (Müll.Arg.) J.Léonard [EUP] | Monguela | 42845 | |
Mifuongongo | R17 | MG489847 | ||||
Mbukuambukua | R16 | MG489846 | Mbukuabukua | |||
Munzundu a mfinda | R3 | MG489838 | Celtis gomphophylla Baker [CAN] | Munzundu a mfinda | 44219 | |
Nkumbi | Entada abyssinica A.Rich. [FAB] | Nsofi | 43942 | |||
Imbrasia obscura (Butler, 1878) | Mansende | R19 | MG489849 | Dichrostachys cinerea (L.) Wight & Arn. [FAB] | Vanga | 44232 |
Mansende | R18 | MG489848 | Macaranga monandra Müll.Arg. [EUP] | Nsasa | 42642 | |
Mansende | Inga edulis Mart. [FAB] | Banana makako | 44781 | |||
Tubula (Kim.) | Ficus spec. [MOR] | Mulembeira | 45865 | |||
Imbrasia truncata Aurivillius, 1908 | Mbambi | R27 | MG489856 | Uapaca vanhouttei De Wild. [PHY] | Musambi | 44171 |
Gonimbrasia (Nudaurelia) alopia (Westwood, 1849) | Mansendenguenia | R8 | MG489839 | Trema orientalis (L.) Blume [CAN] | Mazendenguenia | 44216 |
Gonimbrasia (Nudaurelia) dione (Fabricius, 1793) | Mansende | R40 | MG489862 | Croton mubango Müll.Arg. [EUP] | Mbangobango | 44230 |
Pseudantheraea discrepans (Butler, 1878) | Makaba | R9 | MG489840 | Nsuemba | ||
Micragone cana (Aurivillius, 1893) | Makuakua | R29 | MG489858 | Syzygium guineense (Willd.) DC. [MYRT] | Nkizu | 44138 |
Notodontidae | ||||||
Anaphe panda (Boisduval, 1847) | Mukalakala da mata | R14 | MG489844 | Bridelia micrantha (Hochst.) Baill. [PHY] | Mukalakala | 44224 |
Anaphe panda (Boisduval, 1847) | Munzunzu | R12 | MG489843 | Bridelia micrantha (Hochst.) Baill. [PHY] | Munzunzu | 44224 |
Minzunzu | R11 | MG489842 | Bridelia micrantha (Hochst.) Baill. [PHY] | Munzunzu | 44224 | |
Munzundu | R34 | MG489861 | Bridelia micrantha (Hochst.) Baill. [PHY] | Minzundu | 44224 | |
Anaphe venata Butler, 1878 | Milenda | R1 | MG489837 | Sterculia tragacantha Lindl. [STE] | Milenda | 44004 |
Notodontidae sp. 1 | Minsinda | R22 | MG489852 | Eriosema glomeratum (Guill. & Perr.) Hook.f. [FAB] | Wandu | 43168 |
Notodontidae sp. 2 | Mbanzubanzu | R31 | MG489860 | Allophylus africanus P. Beauv. [SAP] | Mbanzubanzu | 41878 |
Notodontidae sp. 3 | Mindelumuka | R28 | MG489857 | |||
Notodontidae sp. 4 | Minsangula | R30 | MG489859 | Pycnanthus angolensis (Welw.) Warb. [MYRI] | Didila | 44478 |
Erebidae | ||||||
Sciatta inconcisa Walker, 1869 | Milenda | R10 | MG489841 | Ficus bubu Warb. [MOR] | Mindelemuka | 44223 |
Lasiocampidae | ||||||
Gastroplakaeis rubroanalis Wichgraf, 1913 | Mbuokutu | R26 | MG489855 | Mbuokutu | ||
COLEOPTERA Curculionidae | ||||||
Rhynchophorus phoenicis (Fabricius, 1801) | Larva: Nsombe Chrysalis: Kinkekete Imago: Kinkakala | Raphia spec. [ARE] | Bordão | F_60 | ||
ORTHOPTERA Gryllidae | ||||||
Brachytrupes membranaceus (Drury, 1770) | Grilho | MB3108 | MG489863 | different crop plants |
To investigate the quantity and prices of the offered species during several years and seasons, four markets were visited for market analysis. To match prices, central markets in Uíge city and Negage city were compared to markets on their peripheries.
To evaluate the nutritional value of insects, samples from the adjacent municipalities Uíge, Bungo, Puri, Negage and Mucaba were selected in January and February 2014 and analysed for the major nutrients, protein and fat. Water content was calculated through the loss of weight due to freeze drying. All chemicals used were of analytical or higher quality.
Insects usually eaten after evisceration were analysed after removal of the gut as indicated in the results section. All samples were freeze-dried (Beta 1-8K, Martin Christ Gefriertrocknungsanlagen GmbH, Osterode, Germany) and ground for 20 s at 1000 rpm in a Grindomix 200 knife mill (Retsch GmbH, Hahn, Germany). The resulting powders were stored at -18 °C until analysis. Protein analysis was carried out by determination of the nitrogen content according to the Kjeldahl method (System of Büchi Labortechnik AG, Flawil, Switzerland) and application of a conversion factor of F=6.25 for protein content calculation.
For the determination of the fat content, samples were extracted with petroleum ether for 5 h in a Soxhlett extractor. After evaporation of the solvent and drying of the remaining fraction, the fat content was quantified gravimetrically (Matissek et al. 2006).
Our surveys in northern Angola revealed 18 species of insects eaten by local people. Sixteen of them were moth larvae, one a beetle larva and one a cricket. Fourteen species have been identified at species level and another four only at family level (Table
Half of the moth species belonged to Saturniidae (Figs
Photographs of edible larvae of Notodontidae (a–e) and Erebidae (f), collected in the Province Uíge. a Anaphe panda (1) larva (2) male imago b Anaphe venata (1) larva, (2) male imago, cNotodontidae sp. 1 dNotodontidae sp. 2 (left) and eNotodontidae sp. 4 (right) f Sciatta inconcisa (1) larva, (2) male imago.
Larvae of Sciatta inconcisa (Erebidae) were reared to imagoes and identified using
Beside the species mentioned above, we collected dried termite samples in May 2014 at the local market in Uíge. Unfortunately, these termites had already been processed. Therefore, they were neither suitable for DNA-barcoding nor for morphological identification. Though we visited the area during different times of the year, we never met people harvesting termites. For all other insect species, we were able to obtain DNA-barcodes (Table
Along with the sampled larvae, we collected vouchers for the food plants. Their scientific and vernacular names are given in Table
Local differences in climate, rainfall and thus fresh growth of host plant foliage cause a strong seasonality of the appearance of edible caterpillars (Malaisse 2005). In the Province Uíge, the main caterpillar season starts in January and lasts until the end of February (Table
Larvae of Rhynchophorus phoenicis are to be found throughout the year, but with a decrease in availability during the dry season, according to local harvesters. We found Brachytrupes membranaceus from November to February.
The majority of identified caterpillar species live on trees. Children usually collect them, as they are skilful and agile enough to climb up the trees and pick them from the twigs. In addition, men and women going into the field or hunting in the forest focus on larvae in the upper vegetation or individuals which have dropped to lower levels. The characteristic faeces on the ground indicate their presence. Several times, we also detected the quite unsustainable method by which caterpillars are collected - cutting down the whole tree or at least large branches (Fig.
Caterpillars are first washed in water. The long hairs of Anaphe panda must be removed before boiling. Normally, local people singe them off in a frying pan over the fire. The gut of the collected Saturniidae caterpillars, except Cirina forda, has to be removed because host plants, according to the statements of interviewed persons, contain toxic substances (or rather the faeces do) which spoil the flavour. Since several host plant species belong to the plant family Euphorbiaceae, well-known for their poisonous secondary compounds (
The high fat content of the African palm weevil Rhynchophorus phoenicis enables it to be prepared easily by cutting open the larvae and frying it. Crickets of Brachytrupes membranaceus are strung on a wooden stick, roasted over a fire and later sold at the markets.
Alphabetical order of insect species with vegetation unit, collection date, GPS coordinates (DMS); map ID according to Fig.
Insect species | Vegetation unit | Municipality | Collection date | Eastern longitude | Southern latitude | Level [m] | ID in map |
---|---|---|---|---|---|---|---|
Anaphe panda | Forest | Uíge | 26.i.2014 | 14°57'40"E, 7°37'00"S | 1.000 | U | |
Forest | Bungo | 06.ii.2014 | 15°10'23"E, 7°25'59"S | 1.244 | B | ||
Forest | Uíge | 06.ii.2014 | 15°05'07"E, 7°27'05"S | 909 | U | ||
Anaphe venata | Village | Damba | 25.ii.2015 | 15°07'47"E, 6°55'16"S | 1.061 | D | |
Brachytrupes membranaceus | Field | Negage | 11.xi.2013 | 15°36'29"E, 7°41'13"S | 1.152 | N | |
Cirina forda | Savanna | Puri | 30.i.2014 | 15°36'23"E, 7°41'48"S | 1.085 | P | |
Savanna | Puri | 30.i.2014 | 15°35'32"E, 7°41'40"S | 1.085 | P | ||
Gastroplakaeis rubroanalis | Forest | Quimbele | 20.ii.2015 | 16°17'05"E, 6°31'36"S | 741 | Q | |
Gonimbrasia alopia | Forest | Bungo | 06.ii.2014 | 15°10'23"E, 7°25'59"S | 1.244 | B | |
Forest | Bungo | 17.ii.2015 | 15°10'23"E, 7°25'59"S | 1.244 | B | ||
Gonimbrasia dione | Village | Damba | 28.vii.2015 | 14°55'06"E, 6°51'07"S | 812 | D | |
Imbrasia epimethea | Forest | Uíge | 26.i.2014 | 14°58'46"E, 7°37'47"S | 790 | U | |
Forest | Negage | 28.i.2014 | 15°11'38"E, 7°39'35"S | 1.178 | N | ||
Forest | Uíge | 29.i.2014 | 14°57'33"E, 7°40'48"S | 610 | U | ||
Forest | Uíge | 02.ii.2014 | 14°58'26"E, 7°37'38"S | 859 | U | ||
Forest | Bungo | 06.ii.2014 | 15°10'23"E, 7°25'59"S | 1.244 | B | ||
Forest | Bungo | 06.ii.2014 | 15°09'32"E, 7°24'04"S | 1.244 | B | ||
Forest | Damba | 25.ii.2015 | 15°07'47"E, 6°55'16"S | 1.061 | D | ||
Imbrasia obscura | Forest | Uíge | 27.i.2014 | 14°57'14"E, 7°34'27"S | 813 | U | |
Forest | Uíge | 29.i.2014 | 14°57'34"E, 7°40'32"S | 622 | U | ||
Forest | Uíge | 11.ii.2017 | 15°05'40"E, 7°27'06"S | 937 | U | ||
Forest | Malanje Province | 01.iii.2017 | 16°00'00"E, 9°04'26"S | 1.063 | |||
Imbrasia truncata | Forest | Quimbele | 19.ii.2015 | 16°16'57"E, 6°38'01"S | 801 | Q | |
Micragone cana | Savanna | Damba | 23.ii.2015 | 15°11'22"E, 6°55'10"S | 1.094 | D | |
Pseudantheraea discrepans | Forest | Negage | 08.ii.2014 | 15°11'38"E, 7°39'35"S | 1.178 | N | |
Forest | Quimbele | 20.ii.2015 | 16°17'05"E, 6°31'36"S | 741 | Q | ||
Forest | Damba | 26.ii.2015 | 15°07'47"E, 6°55'16"S | 1.061 | D | ||
Rhynchophorus phoenicis | Market | Uíge | 10.x.2016 | 15°03'27"E, 7°36'48"S | (M) | U | |
Forest | Kangola | 12.xi.2015 | 15°50'20"E, 7°56'53"S | 1.095 | K | ||
Sciatta inconcisa | Savanna | Uíge | 06.ii.2014 | 15°07'07"E, 7°27'05"S | 909 | U | |
Notodontidaesp. 1 | Savanna | Mucaba | 03.ii.2014 | 15°06'23"E, 7°12'53"S | 1.160 | M | |
Notodontidaesp. 2 | Forest | Bungo | 17.ii.2015 | 15°10'23"E, 7°25'59"S | 1.244 | B | |
Notodontidaesp. 3 | Forest | Damba | 25.ii.2015 | 15°07'47"E, 6°55'16"S | 1.061 | D | |
Notodontidaesp. 4 | Forest | Bungo | 17.ii.2015 | 15°10'23"E, 7°25'59"S | 1.244 | B |
Phenology of collected edible insect species, based on collected samples: grey larvae, black imagoes.
Species | Month | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
I | II | III | IV | V | VI | VII | VIII | IX | X | XI | XII | |
Cirina forda | ||||||||||||
Imbrasia epimethea | ||||||||||||
Imbrasia obscura | ||||||||||||
Imbrasia truncata | ||||||||||||
Gonimbrasia alopia | ||||||||||||
Gonimbrasia dione | ||||||||||||
Pseudantherea discrepans | ||||||||||||
Micragone cana | ||||||||||||
Anaphe panda | ||||||||||||
Anaphe venata | ||||||||||||
Sciatta inconcisa | ||||||||||||
Notodontidae sp. 1 | ||||||||||||
Notodontidae sp. 2 | ||||||||||||
Notodontidae sp. 3 | ||||||||||||
Notodontidae sp. 4 | ||||||||||||
Gastroplakaeis rubroanalis | ||||||||||||
Rhynchophorus phoenicis | ||||||||||||
Brachytrupes membranaceus |
Edible caterpillars have different local names in the Bantu-language Kikongo, which is spoken by the Bakongo ethnic group in Uíge. In the various research areas, the general terms vary: in the municipality of Uíge, it is called mankoko, whereas in the municipality of Damba local people describe it as impiatu. In the northern municipality of Quimbele, which borders the Democratic Republic of Congo, people name caterpillars as nvukwa or mihuka. Furthermore, local taxonomy divides caterpillar species into mazende (caterpillars with spines), mazende mika (caterpillars with spines and hairs) and mvuka, mihuka or huka (caterpillars without spines or hairs).
Local names on species level often refer to the main food plants, which appear to be similar throughout Africa, wherever caterpillars are eaten (
Interestingly, makuakua (kwâkwa) translated from Kikongo means caterpillar with long stinging bristles (
As already mentioned, the life cycle of holometabolic insects is often not known. Instead, in the eyes of many local people, larvae and their imagoes share no relation to each other. Nevertheless, the connection between caterpillars and birds is drawn. With the beginning of the rainy season in October, migratory birds return and within their beaks, they often bring along caterpillars. A symbol for the concurrent starting season of caterpillars is a bird which sings “makoko é” – translated from Portuguese and, in the figurative sense, it means “the caterpillar season starts”. Due to its call, this bird could probably be Klaas´s Cuckoo (Chrysococcyx klaas) as cuckoos are also major consumers of caterpillars (
Some insect species are commonly offered for sale at local markets. After collection and boiling in salt water, the larvae of Saturniidae or Notodontidae are dried in the sun. The dried larvae of Cirina forda are found at the most important city market in the provincial capital, Uíge, throughout the whole year until the new season starts, whereas Imbrasia epimethea and Anaphe panda are offered only at a certain time. Prices vary depending on market, quantity and the variety on offer from the sellers. Women selling these larvae also often offer beans and peanuts.
From 2013/2014 to 2016/2017, we noticed a significant increase in prices of one caterpillar species. While in 2013 and 2014, one kilo of Cirina forda was sold for 2 to a maximum of 3 US$, in 2016 and 2017 the prices had already doubled to 6-7 US$, irrespective of whether larvae were alive or dried.
It is hard to find caterpillar species other than those already mentioned at local markets. During the caterpillar season, Pseudanthera discrepans, Imbrasia obscura, Imbrasia epimethea and Anaphe panda are frequently found. As Pseudanthera discrepans and Imbrasia obscura are comparatively large larvae, prices are higher (0.5 US$ for 10 units) than for gregarious species like Imbrasia epimethea and Anaphe panda, which always occur in large quantities (0.5 US$ for 50 units). Since these species are rarely sold, accurate statements about distribution and trends in their occurrence are not possible. In our study, 11 of the 18 insect species are exclusively consumed in the villages where they were collected. However during the caterpillar season in January and February, while passing through rural areas by car, it is possible to buy some recently collected caterpillars in plastic bags offered by children (roadside vendors). A quantitative analysis of the percentage of caterpillars sold at local markets is still not possible. Nevertheless it can be said that the occurrence of different insect species represents a key source of income for local people. Prices are relatively high, comparing one kilo of Imbrasia epimethea or Cirina forda (6 to 7 US$) with one kilo of beans and peanuts (3 to 4 US$) at the same market in Uíge city. Moreover, these caterpillar species are simply collected from the wild while beans and peanuts need to be cultivated.
Larvae of Rhynchophorus phoenicis are also sold the whole year round and priced at 4 pieces for 1US$ which is relatively expensive.
Table
Composition of major nutrients. Values per 100 g dry matter, moisture per 100 g fresh weight; indices give the number of analyses asingle, bdouble, ctriple, dquadruple, esextuple; d.m.: dry matter,1:
moisture [g/100 g] | protein [g/100 g d.m.] | fat [g/100 g d.m.] | ||||
---|---|---|---|---|---|---|
Lepidoptera: Saturniidae | references | references | references | |||
Cirina forda | 79.4 +- 3.8b | 73.01 | 57.8 +- 1.1d | 62.32 | 13.1 +- 3.6b | 12.52 |
51.91 | 13.41 | |||||
74.410 | 14.310 | |||||
Imbrasia epimethea without gut | 79.8 +- 3.2c | 93.03 | 73.14 | 6.4 +- 3.8d | 5.94 | |
85.01 | 64.52 | 9.12 | ||||
58.13 | 12.43 | |||||
65.91 | 14.21 | |||||
Imbrasia obscura without gut | 83.0 +- 1.0b | 9.05 | 62.3 +- 3.4d | 53.55 | 5.4 +- 3.3c | 12.25 |
Gonimbrasia alopia without gut | 85.7a | 62.0 +- 0.6b | 1.9a | |||
Pseudantheraea discrepans without gut | 72.2a | 48.9 +- 0.8b | 21.3 +- 0.9b | |||
Notodontidae | ||||||
Anaphe panda | 83.4 +- 0.1b | 73.91 | 53.2 +- 1.3d | 45.61 | 5.6 +- 3.0b | 35.01 |
Notodontidae sp. 1 | 79.5a | 41.4 +- 0.4b | 10.1a | |||
Erebidae | ||||||
Sciatta inconcisa | 73.7a | 46.2 +- 0.6b | 28.02a | |||
COLEOPTERA Curculionidae | ||||||
Rhynchophorus phoenicis | 76.8a | 32.8 +- 0.3d | 56.62 | 38.2 +- 1.1b | 12.02 | |
77.41 | 42.61 | 20.21 | ||||
89.25 | 22.85 | 46.75 | ||||
60.46 | 25.36 | 69.96 | ||||
64.77 | 28.07 | 62.07 | ||||
61.98 | 22.08 | 66.48 | ||||
38.612 | 19.512 | |||||
ORTHOPTERA Gryllidae | ||||||
Brachytrupes membranaceus ‘native’ ‘grilled’ | 68.6a | 44.39 | 61.6 +- 0.3b | 35.29 | 11.9a | 47.69 |
63.49 | 36.69 | |||||
5.3a | 14.29 | 63.1 +- 1.1d | 35.110 | 32.3 +- 0.1b | 53.110 | |
47.911 | 21.311 |
We recorded 18 insect species eaten by humans in northern Angola, 14 species for the first time from Angola and Sciatta inconcisa and Gastroplakaeis rubroanalis for the first time as edible insects. Considering all records about edible insects from Angola together with our results, in total 38 insect species are used as sources of food. This number is more or less equal to those of neighbouring provinces, e.g. 30 species in Kwango (
Besides the species recorded as edible in Northern Angola, we also found imagoes of a further three saturniid species attracted by artificial lights during the night, the larvae of which are known from the Democratic Republic of Congo to be edible. These are Gonimbrasia (Nudaurelia) eblis Streck, 1876, G. (N.) melanops (Bouvier, 1930) and Melanoceranereis (Rothschild, 1898) (
Some of the species consumed in Northern Angola are widely used in Africa. People eat caterpillars of Cirina forda from Togo (
A major issue in studying edible insects is the difficulty with identification of the species. For many of the relevant species, information in identification keys and/or DNA-databases is not yet available. Identification is further hampered by the fact that insect identification largely focuses on the imagoes rather than on larvae. This necessitates rearing the individuals until adult stage or by using methods such as DNA-Barcoding. Furthermore, changes of nomenclature such as of synonyms and changed genus combinations complicate the comparison of results obtained in different countries and during different decades. In the genus Imbrasia, we have found a situation which deserves taxonomic revision. On the one hand, there are very different morpho-types of larvae (Figs b1, c1, d1), while on the other hand, adults displaying the morpho-type of I. ertli Rebel, 1904 and I. obscura are identical in the DNA-barcode.
For Congo-Brazzaville,
Traditional harvesting methods and even host plant manipulations described by
Due to different climatic conditions, the phenology of insect life cycles observed in our study area partly deviates from adjacent regions. In the region Bas-Congo (Democratic Republic of Congo), the caterpillar season lasts longer, from November to February (
The appearance of larvae of Gonimbrasia dione in July 2015 in the Uíge Province therefore was surprising. According to the respondents, a few other caterpillar species also occur outside the caterpillar season in February.
Larvae of Rhynchophorus phoenicis occur throughout the year. Differences in harvested grub quantities between dry and rainy season were also described for Nigeria, varying up to fourfold in the rainy season (
Due to insufficient data, comparing market analyses results of prices and income with other countries is difficult. In addition, price analyses are valuable only in the context of each particular gross national product and vary from village level, in markets and online (
In Nigeria, differing prices for larvae of the palm weevil (Rhynchophorus phoenicis) depending on seasons were detected (
Highest protein and fat contents amongst the Lepidoptera are found for the Saturniidae ranging from 50 to 65% protein and 2 to 21% fat per 100 g dry matter. The data obtained for Cirina forda and Imbrasia epimethea accord especially well with those reported in literature (these are also given in Table
To our knowledge, no nutritional data have been published for Gonimbrasia alopia and Pseudantheraea discrepans, which are presented here for the first time. While the main nutrients of Gonimbrasia alopia generally match those of the Saturniidae discussed above, the fat content of Pseudantheraea discrepans exceeds the others by a factor of 2. As the fat content reported in this work tends to be in the lower range of already published data, this should be confirmed by further analyses.
Fewer references than for the Saturniidae are available for the Notodontidae and Erebidae. Thus, to our knowledge, this publication is the first to document moisture, protein and fat contents of Notodontidae sp. 1 and Sciatta inconcisa. Main nutrients for both species are in similar ranges to those reported by
Our results for Rhynchophorus phoenicis fit within the broad range of data already reported in literature (
Our data supports the rating of (traditional African) insects as valuable source of protein and fat for human and animal nutrition, as stated by several authors and organisations (
Possible anti-nutritive aspects have not yet been included in our work. As some caterpillars are known to feed on plants toxic to humans and accumulation of secondary metabolites in insects as repellents has already been documented, this topic should be part of further studies. Microbial and parasitical contamination as well as the allergenic potential should also be considered. However,
People in northern Angola use insects as an important part of their daily diet, at least during a certain season. With this work, we increase the number of documented edible insects in Angola from 24 to 38. Even if we could not quantify consumption of edible insects in Northern Angola, besides the few domestic animals, game and beans, they play an essential role in protein availability for rural people in the province of Uíge living at subsistence levels. Against this background of the importance of the edible insects, it is surprising to face such difficulties for species identification. Integrative taxonomy should be systematically applied in order to improve our knowledge of edible insects for a wider geographic range.
The fieldwork in Angola was supported by a travel fund from the German Academic Exchange Service (DAAD). These published results were obtained in collaboration with the Instituto Nacional da Biodiversidade e Áreas de Conservação (INBAC) of the Ministério do Ambiente da República de Angola. We thank the administration and the staff of the University of Kimpa Vita in Uíge for logistical support during the stay in Angola. We are grateful for support on the identification of species to Stefan Naumann (Berlin) for Saturniidae, Christian Schmidt for the cricket and Francesca Vegliante for noctuoid larvae. We thank Manuela Bartel, Théo Leger and Franziska Bauer (Senckenberg Museum of Zoology Dresden) for technical support. Andreas Kempe designed the illustrations of the figures. Last but not least, we thank Paul Latham for his helpful review on this manuscript.