Fruits, 2016, vol. 71(6), p.

341-361

c Cirad / EDP Sciences 2016
DOI: 10.1051/fruits/2016027
Available online at:
www.fruits-journal.org

Review article

Influence of environmental factors and production practices

on the growth and productivity of pawpaw (Carica papaya L.)
in south western Nigeria – A review
Olusegun Olufemi Olubode, Olubukola Motunrayo Odeyemi and Isaac Oreoluwa Olatokunbo Aiyelaagbe
Department of Horticulture, Federal University of Agriculture, Abeokuta, Nigeria

Received 27 March 2015 – Accepted 20 April 2016

Abstract – Introduction. Maximizing the production and productivity of pawpaw (Carica papaya L.) under rain-fed
conditions requires a better understanding of the crop, which in turn will enhance its acceptability among fruit growers in
the tropics. Materials and methods. This paper reviews the important limitations observed in the production practices,
assesses the various factors that contribute to pawpaw productivity and evaluates the potential to optimize the crop
development, its management and economic outputs. Results and discussion. The number of leaves and plant leaf area
index are very responsive to growing conditions but more research is needed on the effect of canopy variation between
cultivars. Studies on pawpaw root systems are few, especially the impact of different soil types on rooting volume,
despite their essential role in the plant growth. As a long duration crop with replant problems, early inter-planting with
annuals and crop rotation or inclusion with compatible crops are discussed. Successful inter-planting requires plant
spacing suitable for the plant architecture of various cultivars as well as appropriate plant population and time of inter-
planting with secondary crops. Conclusion. Optimizing pawpaw management can improve the economic performance
of this underutilized crop and increase the benefits accruable from its adoption by fruit growers.

Keywords: Nigeria / papaya / Carica papaya / fruit production / cropping system / postharvest management / shelf life

Résumé – Influence des facteurs environnementaux et des pratiques de production sur la croissance et la pro-
ductivité de la papaye (Carica papaya L.) dans le sud-ouest du Nigeria – Revue de synthèse. Introduction. Maxi-
miser la production et la productivité du papayer (Carica papaya L.) en conditions pluviales nécessite une meilleure
compréhension de la culture, ce qui permettra d’améliorer son acceptabilité par les producteurs de fruits sous les tro-
piques. Matériels et méthodes. Cet article examine les contraintes majeures observées dans les pratiques de produc-
tion, évalue les différents facteurs qui contribuent à la productivité du papayer et évalue le potentiel d’optimisation
du développement, de gestion et de production économique de cette culture. Résultats et discussion. Le nombre de
feuilles et l’indice de surface foliaire de la plante sont des paramètres très sensibles aux conditions de croissance, encore
qu’il reste nécessaire d’étudier l’effet de la variation du volume de feuillage entre cultivars. Les études sur le système
racinaire du papayer sont peu nombreuses, en particulier l’étude de l’impact des différents types de sol sur le volume
de l’enracinement, en dépit de son rôle dans la croissance des plantes. En tant que culture de longue durée posant des
problèmes de replantation, les principes d’une culture annuelle précoce associée, des cultures compatibles en rotation
ou en inclusion sont discutés. Une plantation réussie en culture associée nécessite une densité de plants adaptée à l’ar-
chitecture des plantes selon le cultivar, ainsi qu’une densité de peuplement végétal appropriée et une programmation
dans le temps des cultures secondaires intercalaires. Conclusion. Optimiser la gestion du papayer permet d’améliorer
la performance économique de cette production végétale sous-utilisée et d’augmenter les avantages potentiels de son
adoption par les arboriculteurs fruitiers.

Mots clés : Nigéria / papayer / Carica papaya / production fruitière / système de culture / gestion post-récolte /
aptitude à la conservation


Corresponding author: [email protected]
342 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

1 Introduction and perfume industries [20, 21]. Papain is collected by mak-

ing incisions in unripe pawpaw plants. Although fruits weigh-
Pawpaw (Carica papaya L.) is a native of tropical America ing 0.5 to 1.0 kg contain larger amounts of latex, fruits that
from where it was spread throughout the tropical world [1]. As weigh 1 to 2 kg ripen while those between 200 and 300 g stop
an important agricultural export for developing countries, the developing after latex extraction [22]. The papain extracted
export revenues of the fruit provide a livelihood for thousands from fruit ranges between 4 and 6 g fruit−1 equivalent to 250–
of people, and contribute to the growing supply of healthy 300 kg ha−1 [23]. The latex, a sticky emulsion that exudes
food products in international markets [2]. The nutritional upon damage from specialized canals occurs in about 10%
importance of fruit crops has been well documented [3–8]. of flowering plant species, tends to be more phytochemically
The appropriate intake of essential vitamins and mineral ele- diverse than resins, mucilages, and gums, and often contains
ments contained in the fruit is emphasized as important for the complex mixtures of terpenoids, phenolics, proteins, and al-
maintenance of human health [9, 10]. Among the fruit crops kaloids [24, 25]. Latex fractions from ten latex producing fruit
that supply health-supporting nutritional daily intake is paw- species: Spondias dulcis (ambarella, “amra” in Tamil), Diospy-
paw [11]. It is reported that consumption of 90 g and 135 g ros melanoxylon (East Indian ebony, “tendu” in Hindi), Termi-
of pawpaw everyday will meet the dietary allowances of vi- nalia bellirica (Belleric, “bahera” in Marathi ), Ficus glom-
tamin A recommended by the USDA for children and adults, erata (Indian fig tree or gular), Phyllanthus emblica (emblic
respectively [12]. Pawpaw has a good amount of minerals and or myrobalan, “awla” in Marathi), Thevetia neriifolia (yellow
carotene; it is regarded as a good source of iron, calcium, vi- oleander or lucky nut in the West Indies), Carica papaya (“pa-
tamins A, B and C. Nonetheless, its carotenoid content is low pita” in Hindi), Calotropis procera (kapok tree or Sodom ap-
compared with mango and tomato [6]. Pawpaw is also valued ple), Ficus benghalensis (Indian banyan, “baut” in Bengali),
for its medicinal properties [13]. Various studies have estab- and Artocarpus heterophyllus (jakfruit, “kathal” in Bengali),
lished the potential use of both latex and its components as evaluated for their potency against microbial infections, regis-
valuable sources of medicinal products that can be used for tered significantly higher growth inhibition than that of broad
treatment of life threatening infectious diseases [14]. spectrum antimicrobial drugs [26]. Dried pawpaw latex con-
The world pawpaw production was estimated in 2010 [15] tained higher amounts of crude protein (57.24 ± 0.69%), fol-
at 11,223,031 metric tons (t), including 4,713,800 t from India lowed by moisture (17.76 ± 0.09%), ash (7.00 ± 0.01%), crude
(38.61%), 1,871,300 t from Brazil (17.50%), 703,800 t from fat (5.21 ± 0.13%) and crude fibre (0.67 ± 0.09%). In the en-
Nigeria (6.79%), Indonesia (695,214 t), Mexico (616, 215 t) zyme analysis, papain had protease activity of 2,655 units g−1
and Ethiopia (232,400 t). In 2010 the production was 7.26% at pH 5.5 and 285 units g−1 at pH 9.0 [27]. With an estima-
higher than in 2009, and 34.82% higher than in 2002 [2, 15]. tion of 515.6 USD profits obtainable per hectare per year, pro-
Asia has been the leading pawpaw producing region, ac- duction of papain latex is an economically important alternate
counting for 52.55% of the global production between 2008 product of pawpaw. Nonetheless, pawpaw cultivars differ in
and 2010, followed by South America (23.09%) and Africa papain yield depending on fruit shape, stage of maturity, sea-
(13.16%) [2, 15, 16]. The biggest increase in global pawpaw son of tapping, tapping time of the day, pattern of tapping, and
production occurred between 2009 and 2010, as production frequency of tapping [28, 29]. The repeated use of ethephon
in India increased by 20.50% following a combination of in- applications in coconut oil at 37mM has been shown to in-
creased planted area, improved genetics, and better manage- crease papain yield [30] as cited by [28, 29]. Among the tested
ment. The total exports in 2009 were estimated at 268,476 t, a varieties, ‘CO-6’ was found better for fresh weight as well as
31.5% rise over the weight exported in 2002, with an estimated dry weight of latex as well as fresh and dry yield of papain in
value of about $197.2 million [2]. Other countries involved in 80 days old fruit [31].
commercial pawpaw production for papain include Sri Lanka In the production of rain-fed crops in the semi-arid trop-
and Tanzania. ics, large variations in crops occur in response to the fluctua-
Production of fresh fruit per hectare differs among culti- tions in seasonal rainfall. Hence, in dealing with the variabil-
vars. The choice of cultivar to grow depends on the required ity of rainfall both within and between seasons, it is critical
production type or use to which the fruits is to be put [17]. to identify strategies that can sustain high levels of production
For local fresh fruit consumption or supplies to distant mar- for rain-fed regions [32]. Considerable uncertainty still exists
ket indices such as fruit quality, flesh color, taste and firmness, on how crop species will respond to the observed alterations in
and consumer preference count. Generally, the dioecious paw- global temperature and precipitation patterns [33–35] which
paw cultivars are preferred for extraction of papain because the pose significant threats to their existence and productivity. Im-
yields and proteolytic activity of the crude papain from the fe- provement of crop yields in the tropical environment where
male fruits are greater than those of the hermaphrodites [18]. low yields and low quality confront growers will require ma-
However, for commercial fruit planting, hermaphrodite plants nipulation of important growth factors such as supplemental
from Solo group of pawpaw are preferred because they pro- irrigation, plant/soil nutrition, and light and temperature, and
duce pear-shaped fruits which have thicker flesh and smaller this should be an important aim of research [36]. Although
internal cavity than fruits from female plants [19]. Chovatia et al. [31] reported no significant difference among
The industrial importance of pawpaw lies in its produc- varieties for number of fruits per plant and fruit yield, Olubode
tion of papain and other related proteolytic enzymes such as et al. [37] reported that the ‘Homestead selection’ variety had
chymo-papain. Papain, a thiol protease which is abundant in significantly fewer fruits but greater fruit yield than ‘Sunrise
the milky latex of fruits, is used for food and for the textile Solo’.
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 343

Fleshy and hollow berry fruit varies in size from moder- by grafting and cutting [43] cited in [41], economic consid-
ate to large. Fruits formed from female flowers are oblong to erations indicate that pawpaw is better propagated from seeds
nearly spherical but those formed from bisexual flowers are which abound in the fruits. Moreover, intensive propagation
pear-shaped, cylindrical or grooved. Marketable fruits weigh of clonal material can be achieved through tissue culture, al-
from 0.5 to 2.0 kg [3] and are 10 to 20 cm long. The thin though this is rarely practised because most people engaged
green skin turns yellow at the bottom when maturity sets in. in pawpaw cultivation are resource-poor. Pawpaw is therefore
The flesh is yellow to orange, in some cultivars reddish, and commercially propagated by seed [44]. Being open pollinated,
has a pleasant flavour. Around the cavity lie a thousand or cross pollination often results in a loss of varietal purity [45].
more black seeds, but seedless fruit also occur. Twenty air- Genetics × Environment interactions also often produce a wide
dried seeds weigh about 1 g [38]. array of modified forms, so also the number and types of mod-
Pawpaw has a tremendous yield potential due to its preco- ifications [4]. Consequently, special breeding programmes and
cious bearing and indeterminate growth habit with simultane- experimental designs are needed to distinguish genotypic from
ous vegetative growth, flowering and fruiting [39]. The short- phenotypic variation in pawpaw [46].
lived, near herbaceous, soft woody perennial fruit crop has The irregular and slow germination due to the physiologi-
trees that bear early and supply fruits continuously through- cal quality of pawpaw seeds constitutes an obstacle to pawpaw
out the year. As a trade commodity with world-wide pro- propagation Among the problems observed are the influence
duction, adequate knowledge of pawpaw responses to soil of harvest season on seed quality [47]; postharvest storage of
moisture regimes either in monoculture or polyculture, vari- fruit [48] the presence of sarcotesta [47], and the presence
ous intercropping systems, and the application of conventional of inhibitory compounds in the seed structures [49]. ‘Sun-
and/or organic farming practices for improved farm manage- rise Solo’ pawpaw seeds that had lower density seeds were
ment practices will enable growers to manipulate the crop for observed to have abnormal embryos [50]. High physiological
higher productivity. Although production, especially in tropi- quality seed was obtained from the central portion of fruits at
cal Africa including Nigeria, has hitherto been limited to vol- the fifth (75% maturation) and final maturation (100% mat-
unteer crops located in home gardens or scattered in open uration) stages [51], and postharvest maturity of fruit which
fields [17], recently there has been the planting of medium improved the physiological quality of pawpaw seeds caused
to large scale pawpaw orchards. These produce large consign- a reduction in dormant and non-viable seeds However, an X-
ments of fruit destined for urban centres such as Lagos and ray test proved to be adequate in evaluating the morphological
Port Harcourt in the south of Nigeria, and Abuja and Kaduna quality of pawpaw seed, thus distinguishing between empty
in the North. Some of the fruit also contribute to Nigeria’s for- seeds and seeds with normal embryos [51].
eign exchange [40, 41].
In their critical review of research findings from ex-
periments on indicators and methods using intercropping, 2.2 Germination and seedling growth rates
Connolly et al. [42] observed that two-thirds of the experi-
ments were carried out on research station, only 10% on farm Temperature is one of the best indicators among the cli-
and 24% in undefined location, about half of which were with matic factors that determine the establishment of pawpaw;
annual species only and only about one third involved at least hence, pawpaw trees grow faster in warmer regions, and the
one perennial species including banana (Musa spp.) as a fruit fruit is of better quality than that in cooler regions [52–54].
crop. This review confirms the paucity of information on inter- Moreover, temperature is an important factor that controls
cropping systems involving perennial crops such as pawpaw. changes in crop development from germination and emergence
Many problems confront pawpaw growers, among which through vegetative growth to floral initiation and reproductive
are the unpredictability of environmental conditions, aggra- growth [55]. Hence in regions where temperatures drop below
vated by climate change, leading to significant adverse effects 15 ◦ C, the growth of pawpaw trees is curtailed; thus, no flow-
on growth and yield, and to dwindling revenues. There is the ering occurs, fruit maturation is delayed, and most leaves are
possibility that deploying interventions such as intercropping shed, which causes sunburn of exposed fruit [56, 57]. Further-
with compatible annual crops, with timed introduction of se- more, every phase of a fruit crop is moisture sensitive, although
lected intercrops at appropriate population levels could lead to the degree of moisture sensitivity differs [8]. Thus a perennial
effective and efficient use of resources to maximize component nature, with part of the life cycle spanning the dry season un-
crops production and cropping system productivity. This arti- der rain-fed condition, exposes the crop to soil moisture stress
cle identifies aspects of pawpaw based cropping systems that with widely reported deleterious effects on growth, develop-
require further research. ment and yield [41, 58–60].
The critical water potentials for pawpaw seed germination,
seedling growth, vegetative growth, flowering, fruiting phase,
2 Vegetative growth flowering through fruiting were reported to be –0.01, –0.02, –
0.02, –0.20, –0.20, –0.02 MPa, respectively [41]. Allowing soil
moisture to deplete cyclically below –0.02 MPa soil water po-
2.1 Modern propagation methods tential by watering once in 11 days retarded growth of ‘Home-
stead selection’ pawpaw seedlings in the nursery and delayed
Although true-to-type pawpaw plants that bear earlier, attainment of transplantable size [61], while drought imposed
lower and longer can be obtained through vegetative means by withholding irrigation at the fruit set stage decreased leaf
344 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

area, total dry matter accumulation, fruit set and fruit weight
of field grown ‘Homestead selection’ pawpaw [62]. Although
a moisture level that is adequate for germination of some seeds
may be either insufficient or excessive for others; thus, with-
holding water for 6–9 days before watering delayed and de-
creased germination of ‘Homestead selection’ pawpaw seeds
compared with those watered daily, but enhanced the germina-
tion of ‘Allahabad Safela’ guava (Psidium guajava L.) [41,63].
The reports by Aiyelaagbe et al. [64] and Rice et al. [65] in-
dicated that marked reductions in water availability in soils
tended to limit bud initiation in many fruits, including paw-
paw, where both leaf and flower drops were recorded under
pronounced moisture stress. Figure 1. Canopy spread obtained for pawpaw cultivars at early
seedlings stage. CP, NG and HS are code names for ‘Homestead se-
lection’ morphotypes; SR, PS and CG are code names for ‘Sunrise
2.3 Plant architecture and root plasticity
Solo’ morphotypes. Source: Olubode et al. [71].
Crop communities show a sigmoid pattern of growth dur-
ing the growing season. In the early lag phase; growth of
new seedling is proportional to the leaf area index of crops.
As plants increase in size they overlap to an increasing ex-
tent in both the aerial and soil environments where adjacent

(cm2)
plants begin to interfere (compete) with each other for the
limiting resources of light, water, nutrients and CO2 . As a re-
sult, growth rates and morphologies of individual plant change
drastically with density, and each plant produces less than it
would with unlimited space but production from the commu-
nity is optimized. Thus the smallest plants with least resources
become further disadvantaged and die, leading to self-thinning
in crowded communities. The open space now allows for ex-
panded growth of neighbors as explained by Kira plot of 3/2
replacement theory ([66] as cited in [67, 68]). Figure 2. Leaf area (cm2 ) obtained for pawpaw cultivars at early
Morpho-plasticity is the capacity of plant roots to mod- seedlings stage. CP, NG and HS are code names for ‘Homestead se-
ify their morphology in response to the soil environment [69]. lection’ morphotypes; SR, PS and CG are code names for ‘Sunrise
Morpho-plasticity includes situations where crop architecture Solo’ morphotypes. Source: Olubode et al. [71].
changes result from crop adjustment to increasing density,
along with etiolation, both of which occur when crop densi-
ties, either of monoculture or polyculture (cropping mixtures), 2.4 Fertilizer use in crop productivity
deny crops limited resources. Crop architecture returns to nor-
mal when optimum spacing and resources are available. Paw- 2.4.1 Nutrient-use efficiency
paw roots are highly morpho-plastic and pawpaw plants grown
on hillsides with 70% slope were able to produce ascending In fertilizer trials, the crop yield obtained without added
root growth provided that the soil conditions were favourable fertilizer reveals the amount of nutrient supplied by soil [67].
for root growth [70]. The apparent fertilizer use efficiency is measured by the slope
In a study with three morphotypes, sourced from each of of the yield response to added fertilizer, thus efficiency is large
two cultivars of pawpaw, ‘Homestead selection’ and ‘Sunrise when the nutrient is highly deficient, giving rise to a sharp
Solo’, morphotypes from ‘Homestead selection’ were taller transition between deficiency and adequate supply. In the same
and wider, and had more numerous leaves and longer petiole, way nutrient–use efficiency (NUE) is defined by the biomass
while the morphotypes from ‘Sunrise Solo’ had thicker girth yield curve obtained when plotted as a function of nutrient up-
and wider leaf angulation [71]. Thus cultivars possess distinct take, expressed, for example for nitrogen fertilizer as kg dry
but different plant architecture that changes with time and with matter yield kg−1 N. This relationship follows a diminishing
crop requirement in response to environmental conditions (fig- return but stops short of a plateau. Biomass yield curves can
ures 1–4). Despite this, few recommendations are available for indicate the maximum and minimum above ground biomass
spacing under monoculture conditions and cultivation of paw- that the crop can produce per kg nutrient taken up.
paw in multiple cropping systems adds complexity that could The rapid growth, continuous fruiting and heavy yield of
possibly have a significant effect on production and productiv- pawpaw characterize it as high nutrient exhaustive fruit crop.
ity. Thus appropriate knowledge on pawpaw morphology is a Thus, for high productivity expected nutrient removal at the
prerequisite for devising optimum plant spacing or spatial ar- time of harvest was estimated at about 310, 105, 530, 3332
rangement in crop mixtures for maximum productivity of the and 185 kg ha−1 of N, P, K, Ca and Mg, respectively [72].
cultivars under field conditions. This necessitates judicious application of fertilizers to meet
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 345

A balanced nutrient supply is therefore necessary not only for

obtaining higher and regular yields of better quality fruits but
also for increasing shelf life [39, 79]. The world total fertil-
izer production capacity was estimated as 278 Mt in 2013 with
a total supply of 237 Mt and demand of 183 Mt [80], indi-
cating that fertilizer production should be adequate for crop
production. According to Adedokun and Aiyelaagbe [81], al-
though chemical fertilizers provide readily available nutrients
for plants, their use in tropical agriculture is nonetheless ham-
pered by problems of high cost, scarcity and lack of established
soil testing programmes, while their application increases soil
acidity. Also, NISER [82] confirmed that farmers have limited
access to inorganic fertilizers because of restricted availability,
Figure 3. Leaf angulation obtained for pawpaw cultivars at early procurement and distribution, thereby necessitating the need
seedlings stage. CP, NG and HS are code names for ‘Homestead se- for alternative means of maintaining soil fertility to support
lection’ morphotypes; SR, PS and CG are code names for ‘Sunrise the high yielding crop varieties required to feed the ever- in-
Solo’ morphotypes. Source: Olubode et al. [71]. creasing human population.

2.4.3 Organic fertilizer in crop production

Organic agriculture includes agricultural practices that uti-

lize natural (non-synthetic) nutrient-cycling processes to sus-
tain or regenerate soil quality, such as the use of cover crops,
manures, compost, crop rotation and intercropping [83]. Most
organic farms therefore rely on the sustainable intensifica-
tion of farm management practices that rely on renewable re-
sources, ecological stability, and biodiversity [84] to increase
productivity and lessen environmental degradation [85–87].
The application of organic manures sustains cropping sys-
tems through better nutrient recycling and improvement of soil
Figure 4. Petiole length obtained for pawpaw cultivars at early physical, chemical and biological properties. Many waste and
seedlings stage. CP, NG and HS are code names for ‘Homestead se- by-products, including municipal waste, possess considerable
lection’ morphotypes; SR, PS and CG are code names for ‘Sunrise nutrient value and can be used as organic manure. These are
Solo’ morphotypes. Source: Olubode et al. [71]. often abundant in cities where they may become pollutants es-
pecially to water environment if not properly recycled [88].
Due to the bulky nature of organic manure, their field applica-
the nutritional requirement of the plants [73]. Fertilizer recom- tion may incur high transportation and labor costs. However,
mendations for optimum pawpaw fruit yield for locally avail- these materials are regarded as a safer source of nutrients than
able varieties such as small sized ‘Sunrise Solo’, moderate conventional fertilizers as they are environment friendly mate-
sized ‘Homestead selection’ and large sized ‘Dahomey Large’ rials that through the activation of soil microbial activities re-
in south west Nigeria include 50 g tree−1 month−1 of NPK lease nutrients slowly in synchrony with the crop demand [89].
(15-15-15) [74], and the application of 250 g N plant−1 and Organic manures provide long-term benefits to the soil struc-
150 g P2 O5 plant−1 which produced yields of 38.21 and 39.51 ture and water holding capacity, and are cost effective and
kg plant−1 , respectively, in ‘Sunrise Solo’ [75]. Pawpaw fruit safe [90–92]. Olubode and Fawusi [93] observed the positive
yield, petiole N content and water use efficiency were higher effect of organic manure on pawpaw growth and yield. For ex-
with 450 g than with 150 g N plant−1 in cv. Coorg Honey ample, the application of poultry manure at an optimum appli-
Dew [76]. In order to improve yield and quality of fruit, de- cation rate of 20 t ha−1 significantly increased pawpaw growth
pending on choice of cultivar, farm location and the initial fer- and fruit yields in an organic production system [37, 93].
tility status of the soil, the N requirement will vary from 140 Despite the numerous benefits of organic manure applica-
to 375 g plant−1 , P from 70 to 340 g plant−1 and K from 140 to tion, critics have argued that there are insufficient organically
600 g plant−1 [77]. acceptable fertilizers to produce enough organic food with-
out substantially increasing the land area devoted to agricul-
ture [82, 94, 95]. Also organic crop production is still lacking
2.4.2 Inorganic fertilizer in crop production in terms of yield security and production costs are high com-
pared with conventional and integrated fruit production [96].
Soil qualities known to directly and indirectly affect the However, when practised over a long period, the direct and
nutritional quality of crops include pH, available nutrients, tex- indirect beneficial effects of organic management could con-
ture, organic matter content and soil water relationships [78]. tribute to a higher crop yield on a sustainable basis than is
346 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

obtainable under less sustainable conventional farming. Al- In crop mixture with pawpaw, ‘Homestead selection’ in
though, nutrient supply from organic manure is strongly influ- monoculture showed a correlation between height and girth
enced by prevailing environmental conditions of temperature alone, but ‘Sunrise Solo’ in monoculture and ‘Sunrise Solo’
and water availability and N mineralization will be greatest mixed with either okra or cucumber vegetable showed cor-
during warmer periods when soils are moist [97–100]. Differ- relations among all parameters. The no correlation among
ences in the rate of release of nutrients from different fertilizers parameters measured for ‘Homestead selection’ in cropping
could therefore lead to different C/N ratios in plants and this mixtures indicated the effect of competition among inter-
in turn could lead to difference in the production of secondary crops and that of component crops adaptability to vagaries
metabolites [101]. Depending on the growers’ primary objec- of weather [37]. The results obtained confirmed those previ-
tive, the quantity and quality of resource inputs can be manip- ously reported [103, 105–107] that mathematical relationships
ulated to obtain maximum crop growth, productivity and crop occur among pawpaw growth parameters which can be of sig-
quality. nificant use in growth modelling and productivity predictions.
Pawpaw responds well to fertilization; however the The reproductive parameter, weekly number of flowers, was
‘Homestead selection’ and ‘Sunrise Solo’ pawpaw varieties negatively correlated with other parameters which shows that
did not differ in their nutritional requirements. The optimum as these others increase flowers were either not produced or
yield could be obtained with 10 t ha−1 of a fortified “Type A” shed which is normal since flowers fall when not pollinated.
organo-mineral fertilizer (OMF) [102] while an earlier report The percentage contribution indicated by the regression anal-
found poultry manure at 20 t ha−1 to be the optimum applica- ysis showed that greatest contribution to productivity predic-
tion [37]. Also, the positive effect of OMF on post cropping tion was through plant height (12.6%), girth (11.8%) and num-
soil fertility status was observed whereby soil acidity levels ber of fruits (22.9%) for ‘Homestead selection’ and plant girth
were moderated and decreased by the increased Ca and Na ad- (49.5%), number of fruits (13.7%) and petiole length (10.4%)
dition to the soil [102]. However, the lack of a significant effect for ‘Sunrise Solo’ [37]. The main contributing factors to pro-
of OMF on the post cropping levels of soil nitrogen and phos- ductivity therefore were number of fruits and plant height for
phorus suggested the relative inadequacy of OMF in supplying ‘Homestead selection’ and girth, number of fruits and petiole
these nutrients to pawpaw. This in turn may suggest that the length for ‘Sunrise Solo’ (table II) [37]. Olubode et al. [71]
better performance of pawpaw with OMF than with inorganic obtained taller plants with longer petioles in ‘Homestead se-
NPK fertilizer was due to the supply of nutrients which were lection’ pawpaw but thicker girth and wider leaf angulation in
not present in the NPK (table I) [102]. ‘Sunrise Solo’ which confirms differences in tree architecture
displayed among varieties in the bid to catch sunlight, build
assimilates and enhanced productivity.
3 Reproductive growth
3.2 Flowering and fruiting patterns
3.1 Correlation among growth and yield parameters
Flower initiation plays an important role in pawpaw plant
The relationships among growth parameters, and between development. The initiation of the flower primordial which
growth parameters and yield have been well documented. signals the beginning of the reproductive phase, and the du-
Babu et al. [103] observed a significant positive correlation be- ration between planting the seeds and the first ripe fruit both
tween leaf area and petiole length in the cultivar CO3 and from vary with variety and climate. Aiyelaagbe et al. [64] reported
petiole length obtained a regression equation for determining that for ‘Homestead selection’ variety, flowering commenced
leaf area under field condition. Aiyelaagbe and Fawusi [104] 3 weeks after transplanting of 3 months old seedlings which
obtained a leaf area formula using regression analysis on reached maturity about 10 weeks later. Fruit setting rate has a
mid-rib length. Reddy et al. [105] found a highly signifi- direct relationship with the number of fruit set per plant and
cant correlation between the petiole P concentration and yield; marketable fruit yield [109]. The expected yield is 28 t ha−1
the relationship was strongest with recently matured leaves. year−1 at 15–20 fruits tree−1 [110], with a yield potential of
Balakrishan et al. [106] obtained a highly significant positive 50 t ha−1 year−1 [3], although a range of 30-50 t ha−1 [111]
correlation between dry weight and the product of tree height may occur due to differences in management practices; and,
and stem girth in 10 cultivars of pawpaw. Ghanta et al. [107], while the average life span is estimated to be 25 years [112]
in an experiment using levels of NPK on pawpaw cv. Ranchi only 5 years are considered economic.
obtained a positive and significant correlation between plant As observed with many dioecious species, where male
height and girth at flowering and yield per plant. trees often exceed females in total plant size, plant height,
Using the 6th leaf as an index leaf for plant nutrient anal- growth rates, and frequencies in populations [113–115], taller
ysis, Sanyel et al. [108] observed that the concentrations of female trees have been reported for ‘Homestead selection’
all elements were generally higher in the leaf blade except for whereas significant differences between the sexes was not ob-
K which was higher in the petiole. The leaf blade tissue was served in ‘Sunrise Solo’ [116]. In general, for most plant
the most useful for determining the P, Ca and Mg status of the species, more female than male flowers are developed under
plant while the petiole was best for K, and the optimum sam- favourable conditions, while more male than female flowers
pling time was at flowering. However, both leaf and petiole are developed under stressful conditions [117–119]. How-
were suitable for analysing N status and the optimum sampling ever, among angiosperms, labile sex appears to be more com-
time was 3 months after flowering. mon among dioecious and monoecious plants than among
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 347

Table I. Post cropping soil physical and chemical properties of pawpaw orchards in response to crop mixture with cucumber and applied
organo-mineral fertilizer (OMF) application rates (O.M.: organic matter). Source: Olubode et al. [102].
Soil physical properties Soil chemical properties Macronutrients Micronutrientsy
Treatments
% Sand % Clay % Silt pH (H2 O) % O.M. %N Px Ky Na Ca Mg
Crop varieties
‘Homestead’ 78.6 14.7 6.6 4.7 4.7 0.10 2.53 9.3 4.5 0.86 0.68
‘Sunrise’ 79.3 15.0 5.7 5.0 5.3 0.10 2.73 10.2 4.2 0.84 0.66
LSD var ns ns 0.1 0.05 0.02 ns ns ns ns ns ns
Crop Mixtures
Sole pawpaw 78.4 14.9 6.7 4.7 4.5 0.12 2.37 10.2 4.4 0.81 0.67
Pawpaw in mixture 79.5 14.9 5.5 5.1 5.4 0.07 2.88 9.3 4.3 0.89 0.67
LSD cmix ns ns 0.3 0.05 0.2 ns ns 0.3 0.06 ns ns
Manure Rates
0 t ha−1 OMF 80.3 15.0 4.5 5.1 4.7 0.07 1.53 7.0 4.2 0.79 0.64
10 t ha−1 OMF 80.2 13.9 5.9 4.8 4.7 0.13 2.69 9.8 4.7 0.83 0.66
20 t ha−1 OMF 76.9 15.1 7.9 5.0 6.0 0.13 3.07 11.9 4.4 0.88 0.69
40 t ha−1 OMF 77.6 15.6 6.8 4.7 5.5 0.08 3.86 12.8 5.3 0.92 0.70
NPK 15:15:15 79.6 14.8 5.6 4.7 3.9 0.07 1.99 7.3 3.2 0.83 0.67
LSD fert 0.7 ns 0.5 0.09 0.2 ns 0.2 0.7 0.2 0.03 ns
Interactions
var x cmix * ns ** ns ** ns ns ns ** ns ns
var x fert ns ns ns ns ** ns ** ns ns ns *
cmix x fert * ns * ns * ns ns ns ** * **
var x cmix x fert ns ns ** ns ** ns * ns ** ** ns
x
in ppm; y in cmol kg−1 .
* = significant at P < 0.01, ** = significant at P < 0.05, ns = not significant; var = variety, fert = fertilizer, cmix = crop mixture.

Table II. Regression analysis showing the contribution effect of 3.3 Factors limiting yield – agronomy,
growth and yield parameters to productivity of two accessions of pa- sex identification
paya (B = slope, SE = standard error). Source: Olubode et al. [37].
Parameters ‘Homestead selection’ ‘Sunrise Solo’ Crop productivity is constrained by limiting factors includ-
B SE B SE ing light, water and nutrient. Blackman ([123] cited in [124])
Constant 1.893 1.164 0.947 0.735 stated that plants respond proportionally to increased outputs
of only the most limiting factor until another factor becomes
Girth 0.118 0.384 0.495 0.265
limiting. Von Caemmerer and Farquhar [125] reported that
Nfruit 0.229 –1.354 0.137 0.018 photosynthetic assimilation of CO2 by plants is often limited
Nleaves –0.747 –0.710 –0.309 0.084 at the same time by several plant and environmental factors,
−4 −5
Leaf area 2.928 × 10 0.028 7.291 × 10 0.000 and increasing the supplies of any of these factors increases
Plength –0.148 0.124 0.104 0.018 the growth rate. Inclusive among these factors is the reluc-
NFlower –0.028 0.000 –0.141 0.035 tance of farmers to adopt research results, as reported by Aiye-
PHeight 0.126 0.016 2.819 × 10−2 0.013 laagbe [126] from interviewed farmers who did not adopt the
Crop produce –30.88 0.016 0.038 0.220
recommended practices for fruit growing. Other limiting fac-
tors include difficulty in obtaining seeds of improved varieties,
the problem of excessive cross pollination, poor seed germina-
tion, and difficulty in sex identification of seedling age pawpaw
at planting time.
hermaphrodites in which environmental stress, caused by less Morphology-based sex identification during the seedling
than optimal light, nutrition, weather or water conditions of- or early growth stage is virtually impossible due to a lack
ten favours maleness [120]. As sex expression is regulated by of clearly defined morphological features [127]. Male flow-
plant hormones, it therefore appears that the sexual expres- ers do not produce fruit, and fruit developed from female
sion is controlled by a balance between male promoting and flowers contains less flesh and more seeds than those from
female promoting hormones [121]. Gibberellins are usually hermaphrodites indicating that female plants have less com-
associated with male flowers, while auxins, cytokinins, and mercial value for the production of fruit and seeds [128].
ethylene are usually associated with female flowers [117,121]. To overcome this problem, conventionally, farmers grow two
Nonetheless, pawpaw exhibits wide morphological and bio- or three plants at stake which are later thinned to one upon
logical diversity of its types with prominent sex specific char- flowering to maintain the male to female ratio of 1: 10 in
acters, hence the plants can be either dioecious, monoecious or the field for dioecious plants. For hermaphrodite pawpaw, to
gynodioecious [122]. ensure profitable cultivation, it is necessary to grow more
348 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

hermaphroditic plants than either male or female plants. Sex foliage cover such as juvenile pawpaw in monoculture dur-
is one of the most important factors and traits for plant breed- ing a considerable period of their growth cycle may lose up
ing and production [129]. Attempts made by Ajiboye [116] to 50% of total water use (evapo-transpiration or ET) by soil
and Olubode [130] have not found convincing linkage be- evaporation (Es) [67], while in a crowded community at higher
tween sex and morphological character. However, advances planting densities or in poly-culture, each plant is restricted
in plant breeding using specific genes or markers have been to less than its potential growth rate and final size [85, 145].
able to identify sex at the seedling stage [131]. Several male- The beneficial effects of intercropping systems compared with
hermaphrodite specific markers were independently developed sole cropping with regard to increased productivity, weed con-
by RAPD or AFLP, which were then converted into scar mark- trol and diversification of outputs have been reported by many
ers, e.g., T12 and W11 [132], napf [128], and PSDM [133], researchers [146–151]. The resulting ecological relationships
to distinguish hermaphrodite from female pawpaw seedlings. could be competitive or complementary in nature. However,
These markers have been successfully applied to pawpaw the planting of several crops, which differ in height, root de-
production [127, 134, 135]. Despite the PCR-based sex- velopment, and light requirement, allows for a more efficient
diagnostic methods being widely used, they require modern use of solar energy, soil nutrients, and water [152].
and expensive laboratory facilities and equipment, and might The various ecological relationships in crop mixtures re-
be difficult to perform, depending on the test location, particu- sulting in reduced crop yields have been associated with
larly for field-based genotyping [136]. less soil water exploited by component crops, shading close
to taller crops, phytotoxins in the soil, and competition for
nitrate-nitrogen among component crops [153–157]. Nonethe-
3.4 Yield improvements in organic farming practices less, profitable intercropping of pawpaw specifically is re-
lated to its compatibility with other crops in terms of
The influence of organic matter on soil biological and favourable competition for soil nutrients, soil moisture, and
physical properties is well documented as it affects crop light. Olasantan [148] observed that vegetable crops, includ-
growth and yields, either directly by supplying nutrients or ing cucumber, occupy a valuable ecological niche in tropical
indirectly by modifying soil physical properties [137, 138], agriculture and play a significant role in the eco-physiology
improves soil structures and water retentive capacity [139], of mixed systems. According to Agboola [158], farmers in
increases infiltration rates [140] and decreases soil bulk den- Southern Nigeria have developed a sophisticated system of
sity [141]. However, while a high rate of nutrient release from mixed tree and arable cropping that mimics the multi-storey
fast decomposition occurs only when the organic substrate is vegetation found in a rain forest. Here the tree components
rich in nutrients and has low C:N and C:P ratios, the net nutri- in the mixture are usually not arranged systematically but are
ent release from organic matter is a function of decomposition scattered and sufficiently widely spaced to allow the intro-
ratios of organic matter fractions and uptake of nutrients by duction of arable crops. Hence pawpaw is rarely grown in
the growing biomass [142]. Dipeolu et al. [143] reported that pure stands but usually found in mixtures with other crops
43% of respondents in a survey agreed that organic vegetables of upper storey perennials, usually taller trees such as oil
were more wholesome than conventionally grown ones and palm (Elaeis guineensis Jacq.), middle storey perennials such
33% were prepared to pay 23–27% premium on different or- as Citrus spp., and lower layer annuals and biennials includ-
ganic vegetables. Pawpaw orchards treated with OMF showed ing okra (Abelmoschus esculentus (L.) Moench.), and pepper
significantly (P  0.01) higher P, K, Na and organic matter (Capsicum frutescens L.) [158].
in post cropping soil fertility analysis compared with soil with Successful crop mixtures exploit variation between com-
applied inorganic fertilizer NPK 15:15:15 [102]. The orchards ponent crops by extending the sharing of available resources
planted with cultivation of ‘Homestead crop mixture’ resulted over time and space [159], hence the onset of competition be-
in lower soil bulk density (SBD) and significantly lower or- tween intercrops can be delayed by judicious choice of relative
ganic matter percentage than ‘Sunrise crop mixture’, proba- planting dates. However, physiologically related growth de-
bly due to greater rooting activity. However, post cropping soil pression reported in pawpaw [64,93] at the physiological trans-
Na and Mg was lower after ‘Sunrise crop mixture’ than af- formation from vegetative growth to flowering/fruiting showed
ter ‘Homestead crop mixture’, while soils of orchards planted that ‘Homestead selection’, being a heavy feeder, had a growth
with pawpaw grown in monoculture were higher in SBD [102]. depression that was not observed in ‘Sunrise Solo’ [160],
hence okra planted late (vegetable introduced after pawpaw)
was injurious to ‘Homestead selection’ but not to ‘Sunrise
4 Fruit production and productivity Solo’. This indicates that the most appropriate and safe time
4.1 Crop production under rain-fed conditions to introduce intercrops into pawpaw orchards is at early (veg-
etable introduced before pawpaw) or simultaneous planting
Crop production under rain-fed agriculture is prone to soil periods.
water stress, this notwithstanding, improved productivity and Apart from macro-environmental variation, a micro-
a synergistic effect of optimum combination of organic re- environment exists where competing plant species coexist hav-
sources and fertilizers has been reported to improve water ing vertical leaf profiles that overlap, with both plant species
use efficiency under these conditions [144]. Crop performance shading each other as well as themselves. In such a case,
varies between mono-cropping or multi-cropping systems due either through horizontal space or time, a vertical gradient
to intra- and inter-specific competition. Crops with incomplete in light intensity is created by the plant leaves that form
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 349

the foliage canopy [161, 162]. Plants that deploy leaves high values, and total biomass production for the intercropping of
within the canopy expose them to high irradiance that produces okra with cucumber, implying intrinsic advantages over sole
rapid photosynthesis but pay the considerable energetic cost of crops.
growing and then maintaining tall stems to support these leaves Various studies on cropping systems have reported the re-
compared with plants whose leaves are nearer the ground and tardation effects of intercropping systems on both vegetative
intercept less sunlight and experience slower photosynthesis, and reproductive growth of component crops in mixtures com-
but with the short stems which reduce the energetic cost [163]. pared with monocrops [37, 160, 166, 187, 188, 190]. Intercrop-
Interception of sunlight determines production rate. The poten- ping significantly decreased pawpaw plant height, stem girth,
tial production rate of full cover crops correspond to more than number of leaves, leaf area and canopy spread in the first year
3 g biomass MJ−1 solar radiance and the maximum efficiency while it sustained LER. The significant and non-significant dif-
of energy storage in chemical bonds of biomass is near 5% to- ference in leaf area index (LAI) as a stress indicator at ju-
tal radiation [67]. Light interception by a canopy depends on venile and mature pawpaw stages respectively indicated the
leaf area index (LAI) which has been regarded a stress indi- level of stress imposed on pawpaw cultivated in crop mix-
cator that can be used to compare canopy development over tures and at different times of intercropping [190]. The results
time [164, 165]. Thus, higher total LAI recorded for pawpaw showed that pawpaw could be intercropped with vegetables at
with early cucumber introduction than in monocrop pawpaw the early vegetative stages to sustain land utilization as well
was indicative of an ameliorative influence of cucumber on the as total productivity [37]. The lower growth responses of paw-
environment [166]. This confirmed findings of Ikeorgu [167] paw cultivated as a sole crop than in a mixture with cucumber
and Ossom [168]. However, the observed growth retardation indicated an ameliorative effect of cucumber. However, late in-
of unstressed pawpaw caused by late cucumber introduction troduction of cucumber into pawpaw at a critical growth pe-
could be due to competition for nutrients at a critical growth riod for both crops caused significant growth reduction of both
period of both pawpaw and cucumber which coincided with component crops. ‘Sunrise Solo’ in mixtures produced more
one another [166]. fruit, greater fruit yield and higher vegetable relative yield to-
tal (RYT) value than ‘Homestead selection’ but lower pawpaw
4.2 Crop productivity and economic potentials
RYT value [190]. The lower profit margins obtained from one
intercropping cycle than from sole cultivation was eliminated
Productivity is explicitly defined by the yield of useful with two intercropping times due to the higher yield of cucum-
product per unit land area while considering the efficiency ber with early or simultaneous introduction [166, 190].
of various inputs contributing to the yield [169]. Productivity Intercrop productivity depends on the genetic constitu-
in itself is considered as a very important property of farm- tion of component crops, growth environment (atmospheric
ing system alongside stability and sustainability of the sys- and soil) and agronomic manipulation of the microenviron-
tem. The important criteria involved in making comparisons ment [191]. Hence intercrops are most productive when their
among intercropping systems and in comparing them with sole component crops differ greatly in growth duration so that their
cropping are varied and include such indices as land equiv- maximum requirements for growth resources occur at differ-
alent ratio LER [170–172], aggressivity value [173], relative ent times. “Additive” intercrops are those where growth dura-
crowding coefficient RCC [174], area × time equivalency ra- tions of component crops are similar and the crops compete
tio ATER [176], land equivalency coefficient LEC [176], area more intensely for available resources but may nevertheless
harvest equivalency ratio AHER [177], monetary equivalent be productive, particularly where growth resources are more
ratio MER [178], among others. A widely used indicator of completely captured than in corresponding sole crops, while
productivity or over yielding developed for the Replacement “Replacement” intercrops involve situations where the non-
Series (RS) design [179–181] is the land equivalent ratio replenished growth resources are utilized too rapidly, and the
(LER) [182, 183]. Similar to the relative yield total (RYT) less-competitive component may suffer greatly so no produc-
introduced by De Wit and van den Bergh [184], the LER is tivity gain is experienced in high-yielding environments [191].
defined as:
Yab Yba
LER = +
Yaa Ybb 4.3 Compatibility with component crops
where Yab and Yba are the individual crop yields in intercrop-
ping and Yaa and Ybb are the yields in sole crop [170, 171]. Manipulating resource input into crop mixtures to an op-
Aiyelaagbe and Jolaoso [147] reported an improved Land timum level across seasonal variations highlighted the yield
Equipment Ratio (LER) in pawpaw mixtures with water potential of pawpaw in crop mixtures compared with that ob-
melon (Colocynthus citrullus), okra (Abelmoschus esclentus tainable with sole cropping [192]. With pawpaw mixtures,
Moench), sweet potato (Ipomoea batata), bush greens (Ama- Aiyelaagbe and Jolaoso [147] recorded higher productivity
ranthus hybridus), Jews’ mallow (Corchorus olitorious) and with yield advantages of 3.86, 3.13, 2.06, 1.86, 1.60 and 1.54
scarlet eggplant (Solanum gilo Raddi, syn. S. aethiopicum L.). when intercropped with okra, water-melon, sweet potato, bush
Calculation of land equivalent ratio (LER) showed that re- greens, jews’ mallow and scarlet eggplant, respectively; indi-
sources were used from 17 to 31% more efficiently for growth cating that all the combinations were more advantageous than
by crops in mixtures than by sole crops [185]. John and the monocrop of pawpaw. However, although sweet potato
Mini [186] observed favorable LER, land equivalent coeffi- effectively controlled weeds in pawpaw plots, both sweet
cient LEC, area × time equivalency ratio ATER, aggressivity potato and scarlet eggplant caused marked reduction in the
350 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

Figure 6. Soil moisture content observed under pawpaw/cucumber

Figure 5. Soil moisture content observed under pawpaw varieties. mixtures. HsSole = ‘Homestead selection’ monocrop, SsSole = ‘Sun-
Hs = ‘Homestead selection’; Ss = ‘Sunrise Solo’. Source: Olubode rise Solo’ monocrop, HsCmix = ‘Homestead selection’/cucumber
et al. [102]. mixture, SsCmix = ‘Sunrise Solo’/cucumber mixture. Source: Olu-
bode et al. [102].
fruit yield of pawpaw. Furthermore, intercropping ‘Sunrise
Solo’ with pumpkin (Curcubita maxima) effectively controlled
spear grass (Imperata cylindrica) infestation which was at
par with hoe weeding or application of DelsateTM herbicide.
Among the treatments, only intercropping with white pump-
kin significantly decreased leaf area of papaya with a 13%
decrease in productivity compared with that of chemically
weeded plots [193]. In addition to weed control, intercropping
with pumpkin conserved soil moisture, increased earthworm
activity and decreased diurnal maximum temperature [194].
Weed control in fruits orchard accounts for 30% of operational
costs [195]. Land use system involving [arable crop + teak
+ pawpaw] gave the highest average net return per hectare
after 7 years followed by treatments having subabul grass Figure 7. Soil moisture content observed under applied manure rates.
(Leucaena leucocephala) compared with treatment with only 0 t ha−1 = unfertilized control, organic fertilizers at 10 t ha−1 , 20 t
arable crops [196]. In a field trial, Ler et al. [197] observed that ha−1 and 40 t ha−1 rates, and NPK = inorganic fertilizer at 50 g plant−1
the most productive crop rotation for intercropping in pawpaw month−1 . Source: Olubode et al. [102].
plantation were crop rotations of summer greengram/mustard
greens (Vigna radiata/Brassica juncea) and greengram/wheat
intercrops because of their maximum productivity measured in The ameliorative effect of cucumber on the microclimate
terms of wheat equivalent grain yield. alongside productivity advantages also showed that cucumber
The intercropping of component crops is practised with the could be adopted by pawpaw growers as a relatively com-
sole aim of maximizing plant cooperation for maximum crop patible intercrop of pawpaw [102, 168]. Compatibility be-
yield [198]. Canopy height is one of the important features tween pawpaw and cucumber as intercrops especially occurred
that determine competition ability of plants for light [199]. when higher soil moisture content (figures 5–7) and cooler soil
The taller component crop intercepts the major share of the temperatures (figures 8–10) resulted in more conducive en-
light such that growth rates of the two components will be vironment for improved growth and yield of the component
proportional to the quality of the photosynthetically active ra- crops [168]. The relative yield total (RYT) for okra in two
diation intercepted [200]. The early (okra introduced before years indicated that ‘Sunrise Solo’ was more conducive for
pawpaw) and simultaneous introduction of okra into pawpaw okra productivity than ‘Homestead selection’ [160]. However,
orchards were significantly (P ≤ 0.05) better than late intro- introducing okra late depressed plant height, canopy spread,
duction (okra introduced after pawpaw) in ‘Homestead selec- and leaf area of both ‘Homestead selection’ and ‘Sunrise
tion’ but not in ‘Sunrise Solo’ pawpaw [160], while vegeta- Solo’ pawpaw compared with early or simultaneous introduc-
tive and reproductive growth of ‘Sunrise Solo’ pawpaw, okra tion [160]. Nonetheless, responses of an okra intercrop in ju-
and cucumber component crops were significantly retarded venile pawpaw confirmed an earlier report by Olasantan [201]
(P ≤ 0.05) compared with monocrops in all components of the that in sole and mixed stands with cassava, significant season x
system [166]. Although planting vegetables before pawpaw or population and season x sowing date interactions occur and
planting both simultaneously significantly enhanced flowering there are good prospects and potentials for okra production, but
of pawpaw (P ≤ 0.05) compared with late intercropping, the only with specific planting dates and population densities in
fruit yield of pawpaw was higher (P ≤ 0.05) with late inter- both the early and late rainy seasons in south western Nigeria.
cropping (42.7 t ha−1 ) than with simultaneous and early inter- Moreover, the soil bulk density observed in pawpaw va-
cropping (41.7 and 40.5 t ha−1 , respectively) [166]. rietal trials and in crop mixtures with vegetables showed the
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 351
(°c)

Figure 8. Soil average temperature observed pawpaw varieties. Hs Figure 9. Soil average temperature observed under papaya / cucum-
= ‘Homestead selection’; Ss = ‘Sunrise Solo’. Source: Olubode ber mixtures. HsSole = ‘Homestead’ monocrop, SsSole = ‘Sunrise
et al. [102]. Solo’ monocrop, HsCmix = ‘Homestead Selections’ / cucumber mix-
ture, SsCmix = ‘Sunrise Solo’ / cucumber mixture. (Source: Olubode
et al. [102]).
influence of the different rooting activities of the varieties (fig-
ures 11–13) [102]. This influence appeared related to vari-
etal relative below-ground crop growth responses which con-
tributed to yield differences in the varieties.

4.4 Maximizing the benefits of cropping systems

Apart from savings in the high cost incurred for major

farm operations such as weeding, direct benefits obtained from
intercropping include early income from harvests of annual
vegetable intercrops before the main crop pawpaw is har-
vested [37, 147]. In a three year study, significant varietal dif-
ferences were reported in the response of pawpaw to intercrop- Figure 10. Soil average temperature observed under applied manure
ping with cucumber. ‘Sunrise Solo’, with average fruit weight rates. 0 t ha−1 = unfertilized control, organic fertilizers at 10 t ha−1 ,
20 t ha−1 and 40 t ha−1 rates, and NPK = inorganic fertilizer at 50 g
of 380 g produced 74.8 fruits plant−1 , while ‘Homestead se-
plant−1 month−1 . Source: Olubode et al. [102].
lection’ with average fruit weight of 580 g, produced 44.6
fruits with corresponding fruit yields of 53.3 and 37.9 t ha−1 ,
respectively [192]. Lower profit margins were obtained with
one than with two cycles of intercropping or sole pawpaw due 4.5 Effect of seasonal variation on pawpaw
to higher yield value of cucumber (figures 14, 15) [166, 190]. based cropping system
Yield, economic value, and profit margins obtained for okra
and cucumber differed markedly. The indication was that in- The environmental conditions of temperature and soil
tensification of cropping system by maximizing the available moisture influence the partition of assimilates into either the
land space and time, by using different planting dates for intro- vegetative or reproductive sink. With LAI as a stress indicator,
ducing three months duration vegetable crops in long duration mature ‘Homestead Selection’ had lower vegetative growth in
pawpaw orchard, and by increasing the number cycles of inter- years two and three experiments due to environmental stress
cropping within the same main crop might be more beneficial while mature ‘Sunrise Solo’ recorded no stress across the
than sole or one time intercropping [166]. years [192]. The influence of lower temperature on pawpaw
Highest profit margin was recorded for simultaneous plant- flower induction was observed in a field experiment where the
ing followed by early introduction of okra intercrop in ‘Home- third year, which had the lowest maximum and minimum tem-
stead selection’ pawpaw (46.35 and 43.20%, respectively) or perature, had the highest cumulative number of flowers [192],
in ‘Sunrise Solo’ pawpaw (38.58 and 38.23%, respectively), confirming the report by Olasantan [201] that minimum tem-
while late introduction had the least profit margin in both paw- perature is important in floral induction, although the influ-
paw cultivars [160]. These were all lower than with pawpaw ence of warmer temperature more than moisture availability
intercropped with cucumber. Thus the economic returns cal- was also observed on fruit set [192]. The more flowers, more
culated for mixed pawpaw indicated a profit margin under sole fruits and heavier fruit yield of ‘Sunrise Solo’ and monocrop
pawpaw (64%), sole cucumber (56%) or sole okra (45%) com- pawpaw than of ‘Homestead Selection’ and pawpaw in mix-
pared with 67, 74 and 78% obtained with one, two or three ture indicated the greater yield potential of ‘Sunrise Solo’
cropping times with cucumber [166]. and the yield reduction caused by intense competition with
352 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

Figure 11. Soil bulk density observed under Homestead and Sunrise Figure 12. Soil bulk density observed under papaya/cucumber mix-
pawpaw varieties. Hs = ‘Homestead Selection’; Ss = ‘Sunrise Solo’. tures. HsSole = ‘Homestead’ monocrop, SsSole = ‘Sunrise Solo’
Source: Olubode et al. [102]. monocrop, HsCmix = ‘Homestead Selections’/cucumber mixture,
SsCmix = ‘Sunrise Solo’/cucumber mixture. (Source: Olubode
et al. [102]).
an intercrop for growth resources. Despite the LER > 1.00
recorded over three years (1.37, 1.57, and 1.28) indicating sig-
nificant seasonal differences in productivity responses among
pawpaw varieties, a higher RYT and LER for ‘Sunrise Solo’
and pawpaw/okra mixtures than for ‘Homestead Selection’
and the monocrop pawpaw indicated both the higher produc-
tivity of ‘Sunrise Solo’ and the significant contribution effect
of the okra intercrop in the overall productivity of the crop
mixtures [192].
The high crop production and productivity potentials of
pawpaw, which are near optimum in the even distribution of
environmental moisture in triple peak rainfall pattern of year
two experiment compared to the higher rainfall but with less
even spread of environmental moisture of year three experi-
ment indicated the essence of a balanced pawpaw productiv-
ity requirement [192]. Pawpaw in crop mixtures would need Figure 13. Soil bulk density observed under applied manure rates.
a sustained soil moisture content and/or supplemental mois- 0 t ha−1 = unfertilized control, organic fertilizers at 10 t ha−1 , 20 t
ture application to support component crops and thus alle- ha−1 and 40 t ha−1 rates, and NPK = inorganic fertilizer at 50 g plant−1
viate the competitive needs for moisture in a crowded plant month−1 . Source: Olubode et al. [102].
community as described by Loomis and Connor [67]. For ex-
ample, pawpaw in crop mixtures with cucumber initially had
higher soil moisture, lower temperature and lower bulk den- kept air-dry in airtight containers can retain their viability for
sity than monocrop pawpaw, while under prolonged moisture 2–3 years [203]. Among the most important factors that de-
stress the reverse was obtained. The inclusion of trailing plants termine storage life and final fruit quality is the maturity of
such as cucumber (Cucumis sativus L.) [168] in pawpaw mix- pawpaw fruit at harvest [5], as immature fruits are more sub-
tures provides a conducive soil microclimate including higher ject to shrivelling and mechanical damage, and are of inferior
moisture content, cooler temperatures, and effective weed sup- flavour when ripe. On the other hand, overripe fruits are likely
pression. As pawpaw is highly responsive to soil moisture to become soft and mealy with insipid flavour soon after har-
stress, this would indicate that at certain periods of growth, vest [5]. One of the main causes of postharvest losses is me-
pawpaw would benefit from a compatible companion crop to chanical damage to pawpaw skin through poor handling, un-
stabilize the microclimate in a sustainable manner. suitable containers, improper packaging, and jostling of fruits
during transportation thus causing bruising, cutting, breaking,
impact wounding and other forms of injury [204, 205].
4.6 Fruit handling, postharvest and storage High temperature, low atmospheric humidity and physical
techniques injury alter the natural deterioration rate through physiologi-
cal changes, which can also occur spontaneously by enzymatic
Pawpaw has a high yield potential due to its precocious action leading to over ripening and senescence, a simple aging
bearing and indeterminate growth habit [39]. The storage phenomenon [204]. Ripe, full-color fruit can be held for more
life of harvested pawpaw fruit is short due to dehydration than 1 week at 1–3 ◦ C. Pawpaw fruit at color-turning (break)
losses and rotting leading to revenue losses to farmers en- stage can be stored at 7 ◦ C for 14 days and will ripen normally
gaged in its production [202]. However, pawpaw seeds, when when transferred to room temperature [206, 207]. At 7–10 ◦ C,
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 353

Figure 14. Profit margin (%) obtained for ‘Sunrise’ pawpaw in Figure 15. Profit margin (%) obtained for ‘Homestead selection’
crop mixture with cucumber and okra introduced at different times. and ‘Sunrise’ pawpaw in crop mixture with cucumber introduced
NIT 1 = One Intercropping Time, NIT 2 = Two Intercropping Times, at different times. NIT 1 = One Intercropping Time, NIT 2 = Two
NIT 3 = Three Intercropping Times, SsOkE – ‘Sunrise’/Okra Early, Intercropping Times, NIT 3 = Three Intercropping Times, HsCuE
SsOkS – ‘Sunrise’/Okra Simultaneous, SsOkL – ‘Sunrise’/Okra Late, – ‘Homestead’/Cucumber Early, HsCuS – ‘Homestead’/Cucumber
SsCuE – ‘Sunrise’/Cucumber Early, SsCuS – ‘Sunrise’/Cucumber Simultaneous, HsCuL – ‘Homestead’/Cucumber Late, SsCuE –
Simultaneous, SsCuL – ‘Sunrise’/Cucumber Late„ SsOkM – ‘Sun- ‘Sunrise’/Cucumber Early, SsCuS – ‘Sunrise’/Cucumber Simul-
rise’/Okra Mixture, SsCuM – ‘Sunrise’/Cucumber Mixture, ER – taneous, SsCuL – ‘Sunrise’/Cucumber Late, HsCu – ‘Home-
Early, ST – Simultaneous, LT – Late. (Source: Olubode et al. [166]). stead’/Cucumber Mixture, SsCu – ‘Sunrise’/Cucumber Mixture, ER
– Early, ST – Simultaneous, LT – Late. (Source: Olubode et al. [190]).
storage-life is limited by chilling injury while at 10–13 ◦ C (50–
55 ◦ F) ripening occurs slowly [207]. However, since sugar de-
velops only at the onset of ripening process any attempt to har- was reported to inhibit fungal conidia germination and extend
vest at the earlier stages of fruit maturity meant to achieve bet- pawpaw storage life by 15 days, and reduced the incidence of
ter storage life will be at the expense of quality [208] indicat- weight and firmness loss. Since postharvest cooling removes
ing the reason why pawpaw picked at a quarter to full yellow field heat in fruit, proper cooling should suppress enzymatic
colour taste better [2] and reached peak flavor when the skin degradation, lower water loss in fruit thereby prolonging good
attains 80% yellow color [209] whereas those picked mature- fruit quality before arrival to consumers’ tables [216].
green to one quarter yellow do not increase in sweetness after However, in many developing countries postharvest han-
harvest. dling procedures are poorly developed and agriculture may be
Pawpaw fruit treated with aqueous seed extract and papain characterized as disjointed because production is not closely
exhibited remarkable mycelial inhibition of fungal pathogen integrated with marketing [217]. The lack of availability
causing pawpaw fruit rot with mean zones of inhibitions be- of proper storage and transportation facilities and improper
tween (0.23–1.73 mM) [210]. Pawpaw fruit coated with aloe handling methods result in high levels of damage during
gel (AG) alone and mixed with pawpaw leaf extract (PLEAG harvesting and transit [218]. Estimated losses which may be
at 1:1 v/v) maintained their shelf life for 12 days and de- regarded as normal at 10% may run up to 80% in develop-
cayed only after 16 days. There was 27% disease incidence ing countries [3]. Hence about 5–25% of the produce (fruit
with AG and only 13% with PLEAG coated fruits compared and vegetables) leaving the farm gates may never be con-
with 100% for the untreated control during the same storage sumed but is thrown away. Underlying these problems is poor
period [211]. The pre-treatment of fruits with hot water fol- government intervention, typical of most tropical areas with
lowed with chlorine can also extend the percentage of pawpaw inadequate extension of information and absence of capac-
fruit successfully preserved by 8% over untreated fruits and ity building programmes to bridge the knowledge gap among
has been a method reported to kill insects and inhibit microbial farming communities. This has been compounded in some
growth [212, 213]. Similarly, the treatment of fruits with cal- countries by an overdependence on non-agricultural sources
cium based salts have extended storage life while sodium salts, of revenue such as oil whereas some governments have suc-
particularly sodium chloride, resulted in both physical and mi- cessfully established functional marketing board that link farm
crobial deterioration of the fruit [214, 215]. Calcium chloride with markets. This is confirmed by Aiyelaagbe [8] reporting
354 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361

that the challenge of raising productivity of horticultural crops ergy evaporative coolant structure (ECS), a humidity cham-
is daunting and only an effective policy environment will allow ber promoted by the NSPRI and described by Babarinsa and
horticulture to contribute effectively to healthier and improved Nwangwa [225] not only reduces the storage temperature but
livelihoods in developing countries such as Nigeria. also increases the relative humidity in storage, essential for
The most important aspect of post-harvest handling is stor- maintaining the freshness of the commodities. The ECS thus
age as the storage life of most fruits is short due to dehy- has potential for use for short term preservation of vegetables
dration, losses and rotting [219]. The most commonly used and fruits soon after harvest [226]. There are several shapes
storage techniques for pawpaw include refrigeration which and sizes of ECS but all utilise the same principle [227] and
controls temperature and humidity by mechanical means; and are ideal for storing fruit in developing country where farm-
controlled atmosphere storage which controls the concentra- ers have limited resources. In addition, ECS are beneficial and
tion of oxygen and carbon dioxide, in addition to temperature convenient for rural farmers because they are cheaper, acces-
and humidity. These methods are both categorised as “high- sible and can store harvested produce well for considerable
tech” and likely to be available only to companies or commu- periods [7, 202, 228]. However, for storage of various farm
nally grouped farmers producing the same varieties for specific products, the ECS design using “metal-in-block” has been re-
markets in medium to high quantities. In contrast, “low-tech” ported as the most efficient method, followed by “pot-in-pot”
storage methods available to individuals include the zero en- while “metal-in-pot” was the least efficient [229]. “Wet-jute-
ergy evaporative coolant structure promoted by the Nigerian box” was also considered a more efficient method than “pot-
Stored Products Research Institute (NISPRIN) in Nigeria [7]. in-pot” for produce preservation [230]. The mean tempera-
ture and relative humidity in ECS storage structures was lower
with 19–26 ◦ C and 89.5%, respectively, than the ambient stor-
4.6.1 Refrigerated storage age conditions of 28–31 ◦ C and 61.14%, respectively, and had
lower product weight loss (5.95%) than in ambient conditions
Ripe pawpaw fruits will store successfully at low temper- (18.39%) [231, 232].
atures. Medina De La Cruz et al. [203] stated that the recom-
mended storage temperature for pawpaw is 10 ◦ C and storage
of unripe pawpaw below this temperature will result in chilling 4.7 Call for new production strategies
injury with symptoms of surface pitting, discoloration of the
peel and flesh, incomplete ripening, poor flavour and increased The observed dwindling revenue from pawpaw fruit pro-
susceptibility to disease. Nonetheless, different maturity stages duction [2, 15] calls for the adoption of new production strate-
require different storage temperatures for shipment. Pawpaw gies to improve productivity and profitability. Improving the
fruits above colour break are held at 8 ◦ C, in which case the poor produce quality and financial losses that result from pro-
fruits keep for 4 weeks, but this temperature is detrimental duce spoilage along the production chain, encountered mainly
for those at mature green stage for which the safe temperature by the rural farmers who produce most of third world produce
appears to be around 10 ◦ C [208], while pawpaw at colour- will need direct government intervention. Produce spoilage
turning stage can be stored at 7 ◦ C for 14 days and will ripen could be temporarily delayed and/or significantly reduced be-
normally when transferred to room temperature [206, 207]. fore delivery to destination points. Farmers need exposure to
modern production techniques and direct government inter-
vention by improving rural extension services will introduce
4.6.2 Controlled atmosphere storage farmers to improved production techniques that will ensure
high grade produce for increased local markets and for export.
Controlled atmosphere storage of pawpaw can be effective
Intervention by direct purchase and distribution of quality har-
only when the CO2 concentration is kept below 1% and it is
vested produce, and the provision of modern storage facilities
used along with low temperature, hot water and ethylene bro-
to the organized sector for prolonged shelf live is also possible
mide treatments [208]. Shelf life extension of 1 to 1.5 days
through organised sharing of manageably sized storage facili-
was obtained when pawpaw were stored at 12 ◦ C in 1 to 1.5%
ties, using larger communal groups and/or agricultural cooper-
O2 for 6 days [220] cited in [221]. Low O2 (1 to 5%), with or
atives/units. Fair and farmers friendly policy will provide en-
without high CO2 (2 to 10%), reduces decay [222] and delays
vironment for improved value chain and protect rural farmers
ripening [206, 223]. High CO2 (30%) adversely affects inter-
from exploitation by aggressive business men. This will result
nal color, aroma, and flavor, while there is no residual effect
in an enhanced produce production and greater productivity
of 10% CO2 on decay control, though skin de-greening is de-
among farmers, improved livelihood for the rural farmers and
layed. Fruit stored at 10 ◦ C and 98% relative humidity and
an increased gross domestic product in the nations.
low pressure of 20 mm Hg, ripened more slowly than fruit at
normal atmospheric pressure. Low-pressure storage appears to
suppress disease development [221, 224].
5 Conclusion

4.6.3 Evaporative Coolant Structure (ECS) Although seasonal variation can have a significant effect
on crop production and productivity, knowledge driven crop-
Compared with the high cost involved in developing ping systems can manipulate production factors to a better ad-
cold storage or controlled atmosphere storage, the zero en- vantage. The identification of compatible crops to maximise
 Olusegun Olufemi Olubode et al.: Fruits 71 (2016) 341–361 355

resource use efficiency and intensification of intercropping [12] OECD (Organisation for Economic Co-operation and
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Cite this article as: Olusegun Olufemi Olubode, Olubukola Motunrayo Odeyemi, Isaac Oreoluwa Olatokunbo Aiyelaagbe . Influence of
environmental factors and production practices on the growth and productivity of pawpaw (Carica papaya L.) in south western Nigeria – A
review. Fruits 71 (2016) 341–361.