The association of bushy legumes with ataúlfo mango by Alejandro Ley de Coss

Research Paper I H J

Indian Horticulture Journal; 5(3/4): 63-69, July-December (2015) ©Indian Society of Advanced Horticulture ISSN: 2249-6823 DI: 169-15-IHJ-2404-2015-14

The Association of Bushy Legumes with ‘Ataúlfo’ Mango (Mangifera indica L.)+ cv. Ataúlfo Affects Reproductive Biology and Enhances Productivity in Mango Plantations in Soconusco, Chiapas, Mexico Marroquín-Agreda, Francisco1*; Gehrke-Velez, Malc Rodney1*A; Pohlan, Jürgen Alfred2 ; Lerma-Molina, José Noé1*; Toledo-Toledo, Ernesto1*; Ley-de Coss, Alejandro1* and Juan Alberto, Rodríguez Morales 1*

Cuerpo Académico - Productividad de Agroecosistemas Tropicales. Facultad de Ciencias Agrícolas, Universidad Autónoma de Chiapas. Entronque Carretera Costera - Pueblo de Huehuetán, Huehuetán, Chiapas, México. CP. 30660. Phone: 1+52(964) 62 7 01 28; Fax: 01 (964) 62 70439. 2Rheinische Friedrich-Wilhelms-Universität Bonn, INRES, Tropischer Pflanzenbau. Auf dem Hügel 6, D-53121 Bonn, Germany e-mail: marroquinf@gmail.com Received: 24 April 2015; Revised accepted: 02 August 2015

ABSTRACT The study analyzes the effect of associating four legumes (Crotalaria spectabilis, Cajanus cajan, Vigna unguiculata and Crotalaria longirostrata) in two spatial arrangements during two mango production cycles on the reproductive biology and productivity of ‘Ataulfo’ mango in the state of Chiapas, Mexico. Variables were measured from July 2011 to April 2013. Legume associations increased the number of floral panicles during the two cycles studied. The Crotalaria spectabilis treatment retained 510 floral panicles versus 359 in the control. Cajanus cajan showed a highly significant masculine/hermaphroditic flower ratio of 79/21 percent. Highest yields were obtained in the Crotalaria spectabilis and Crotalaria longirostrata associations (924 and 1388 kg ha-1 respectively). It is concluded that differences in reproductive variable values and productivity in mango favouring legume scenarios, were due to microclimatic changes and lower temperature fluctuations induced, to the incorporation of nitrogen by the legume rhizobia, to soil humidity and to the incorporation of organic matter. Key words: Mangifera caesia Jack ex Wall, Legume, Association, Ecophysiology, Climate change, Productivity Organoleptic and shelf-life characteristics of Ataúlfo mango (Mangifera caesia Jack ex Wall) have made this cultivar commercially the most important and preferred fruit in the Soconusco region of Chiapas, Mexico (NOM 188 SCFI 2012). As a result there are presently 27,291 hectares planted in Chiapas with an average yield of <1 t ha-1, well below the national average yield of 2.6 t ha-1 (SIAP 2013). Nevertheless,

the state of Chiapas holds the second place regarding nationwide planted area and first place in fresh mango exports to the U.S.A. The most important problem of this fruit from a yield point of view is the low level of fruit set which results in a maximum of three fruits per panicle from an original production of more than 2500 flowers per panicle (Gehrke et al. 2011). Many factors are involved in this phenomenon. Among them are

The specific nomenclature applied to the ‘Ataúlfo’ mango in the official Mexican norm is (Mangifera caesia Jack ex Wall).The authors do not apply this denomination due to the fact that the morphological description of this species is not in accordance with the physical appearance of the specimens of the “Ataúlfo” variety used in the present study. For the purposes of the present study the accepted specific epithet indica is applied.

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Francisco et al. 2015 climate change, indiscriminate use of pesticides, and the simplification of a complex system involving soil, plants and insect life turned it into a simplified system. Among undesired results of this, there is drastic yield reduction in mango, coming from 15 t ha-1 in the 1980‟s to < 1t ha-1 harvested at present. In addition to this there is an urgent need to find and apply alternatives which will return the ecophysiological equilibrium to the orchards. The sub utilized legume species Crotalaria longirostrata and Crotalaria spectabilis are examples of the potential biodiversity available in Chiapas which can be incorporated into the fruit orchards. Some legume genera such as Crotalaria have shown important insecticidal and environmental enhancement properties during their growth and development which include attractive flower forms and colours, flowering time coincident with mango and rambutan flowering, high biomass production above 16 t ha-1 (Marroquin et al. 2007), nitrogen fixation through symbiosis and organic matter incorporation. Hence, it is considered that the association of legumes with high agro ecological value in fruit orchards is an alternative to revert ecophysiological and agro-ecological problems resulting from inappropriate farming methods, and to improve yield and crop quality in the orchards. The present study addresses the issue in order to shed light on the physiological effect of legume interplanting on productive and reproductive responses in Ataulfo mango.

During the field stage four species of legumes (Crotalaria spectabilis Roth, Cajanus cajan (L.) Millsp, Crotalaria longirostrata Hook & Arn and Vigna unguicualata L.) were evaluated, these being seeded in a two metre band within the exterior raindrop area of the mango trees. This spatial arrangementenables analysis of multiple interactions between the orchard trees and the multi-purpose legume bushes in order to compare them with the conventional orchard system typified by intensive herbicide usage. Treatment arrangement and distribution under a random block design as follows: 4 treatments and 8 repetitions (32 mango trees ) for which an experimental area of 2800 m2 (160 × 80 m) was selected setting up 4 blocks, each block consisting of 2 mango trees resulting in 32 experimental units. Field work was done during two mango cycles, each cycle initiated with legume seeding in June (Table 1) and terminated six months later with the harvesting of seeds. Legume biomass was incorporated in the mango tree raindrop area after mango flowering. Ataulfo mango reproductive and productive-phase variables were measured in the field. To this end four vegetative buds were selected in the middle third of each tree at each of the four cardinal points (North, South, East and West) making a total of 16 buds per treatment. Number of floral panicles per tree During the three floral flushes detailed counting of reproductive tissues was done weekly in each of the trees observed. Sex and sex ratio of flowers: Flower sex and number was observed and counted during all floral flushes. Number of fruits set per inflorescence: Floral panicles were selected in each tree at each of the four cardinal points making 32 samplings per treatment and a total of 128 panicles weekly up to physiological maturity and the number of fruits set was recorded for each inflorescence. Yield: Number and weight of fruits per tree was registered at harvest time as was data regarding commercial quality vs. nubbin production. Climate data: An OAKLON data logger was installed in the middle third of each tree in order to measure minimum and maximum relative humidity and temperature at 60 minute intervals. Soil temperature and humidity were measured with a Watermark Soil Moisture sensor placed at the 0-10, 10-20 and 20-30 cm layers within the tree raindrop zone. Information obtained during research was analyzed under descriptive statistical parameters as well as with variance analysis. Data with significant statistical

MATERIALS AND METHODS The study was carried out in an „Ataúlfo‟ mango plantation during the July 2011-April 2012 and July 2012-April 2013 seasons in the municipality of Tapachula, Chiapas, Mexico; geographically located at 14º 55‟ North lat. and 92º 22‟ west long with an altitude of 41 m.a.s.l. Climate is warm humid with abundant rainfall in summer (Aw2 (w”) in according to Köppen modified by Garcia (1988). High temperatures and heavy rainfall are typical in the region. Rainiest months are September and October. Annual rainfall is 2800 mm and mean monthly temperature is 28°C, with a maximum of 37°C and a minimum of 18°C. Soil type is a eutriccambisol with a loamy to clay loam texture and a 3.3% organic matter content in the upper 10 cm and 2.1% in the lower strata. pH is 6.2 without soluble salt problems at depths below two meters. The Ataulfo mango orchard was planted in 2007. Varietal origin and genetic quality wasunknown. Planting density was 32 trees per hectare and planting distance was 20 × 20 m. Indian Horticulture Journal 5(3/4)

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Bushy Legumes Affects Reproductive Biology and Enhances Productivity in Mango differences were submitted to a multiple range medium comparison following the Tukey (α-0.05)

method. Statistical analyses of data were applied using the STATGRAPHICS Centurion XVI program.

Table 1 Legume management in aninterplanted mango orchard Legume crops Agronomic management of associated species 1. Crotalaria spectabilis  Legume seeding: July (C. cajan, C. longirostrata), August (C. spectabilis and V. 2. Crotalaria unguiculata) longirostrata  Planting density: Crotalaria spp & Cajanus cajan 0.70 × 0.10 m and Vigna 3. Cajanus cajan unguiculata 0.70 × 0.40 m (row planted). 4. Vigna unguiculata  1st weed control: post-emergent applicatión 5 days before seeding (DBS) Paraquat (20%) + Diuron (10%), application rate 18%, approx 2 l/ha (180 ml/ 20 l H2O).  2nd weed control: mechanical control (machete) 40 days after seeding (DAS)  Crotalaria and Cajanus harvested in January 5. No legumes  Conventional system (Hand-weeded). 1st weeding post emergence 5 days before (mango monoculture) seeding Paraquat (20%) + Diuron (10%), Application rate 18%, approx 2 l/ha (180 ml/20 l H2O)  2nd Weeding: mechanical control (machete) 40 DAS  3rd weeding post emergence 66 DAS Paraquat (20%) + Diuron (10%), application rate 18%, approx 2 l/ha (180 ml/20 l H2O) unguiculata showed an increase of 162.75 PPT and C. spectabilis only increased 47 PPT despite having shown the highest number of PPT in both cycles. Control treatment produced 27.75 less PPT than in the first cycle, whereas C. cajanus and C. longistrata showed decreases of 187.43 and 73 PPT, respectively. Agro-ecological conditions in the mango-legume system showed no statistical significant differences in either of the two reproductive cycles observed.

RESULTS AND DISCUSSION Number of floral panicles During the first cycle (2011-2012) flowering period lasted eleven weeks producing representative flushes at the 7, 14 and 21 day intervals (November 17, 21 and December 1) following appearance of the first panicles (FPA) (November 11). However, during the second cycle (2012-2013) floral flushes started 14 weeks after FPA (December 2) at intervals of 14, 77 and 84 days following FPA (December 18, and February 23 and 28). No significant differences were observed between treatments as regards FPA, although panicle emergence during the first cycle (2011-2012) came three weeks earlier than in the second cycle (2012-2013). Association with legume bushes enhanced panicle production during both cycles observed. During the first cycle (June 2011-April 2012) trees with the greatest number of panicles were those associated with C. spectabilis (463 panicles per tree (PPT)) and C. longirostrata (462 PPT). Control treatment produced 362 PPT. This difference was even greater in the creeping legume (Vigna unguiculata) treatment which produced the lowest number of PPT (285). During floral flushes in the second cycle (July 2012-April 2013) differences in panicle abundance in the legume associations were much more notable. A maximum of 510 floral panicles for C. spectabilis, followed by 448 for Vigna unguiculata and a minimum of 303 for the control treatment were observed. The effect of legume associations on the number of PPT was more notable during the second cycle. V. Indian Horticulture Journal 5(3/4)

Floral emission and sex ratio in Ataulfo mango/legume associations The association of bushy legumes within the raindrop zone of Ataulfo mango shows a marked influence on the increase of flowers per panicle (FPP) during the two cycles observed. During the first cycle (2011-2012), associations showed differences in the number of flowers emitted. Highest values were observed in the C. spectabilis association (1,766 FPP), followed by Cajanus cajan (1,686 FPP). The opposite occurred in the C. longistrata association and in the control treatment (777 and 715 FPP respectively). The overall number of flowers produced and the bushy legume associations improved with regard to the untreated control despite this decrease. FPP in the C. spectabilis association was 608 and 559 in C. longistrata. The hermaphrodite/masculine flower ratio (Hf/Mf) during the first cycle (2011-2012),showed highest hermaphrodite (Hf) values for the untreated control(73%), followed by the C. spectabilis association (71%) and C. longistrata (63%) However, during the second cycle (2012-2013) all 65

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Francisco et al. 2015 legume/mango associations produced higher Hf percentage values as opposed to the untreated control. During this cycle, C. cajan associations produced 79% hermaphroditic flowers and the C. longistrata association showed 70% Hf production. Untreated control (No cover crop) gave the lowest Hf reading (63%) (Fig 1).

although all the associations had the same performance pattern. Highest abortion rate occurred at 7 to 28 days after anthesis. During the 2012-2013 cycle, bushy legume associations showed the same fruit set performance pattern as the previous cycle in which the highest amount of total fruit drop occurred at 7 to 21 days after anthesis in all treatments. Legume associations increased fruit set, especially Cajanus cajan and C. spectabilis treatments with 2.50 and 2.0 fruits per panicle in comparison with 1.77 in the untreated control (no legume). The Cajanus cajan association showed the lowest temperature variations (without abrupt changes) and C. spectabilis, the lowest temperatures readings (28°C). The highest temperature readings (36°C) were recorded at the control treatment (no legume) during the first days following anthesis (Fig 2). However, differences are not statistically significant.

Fruit set Legume associations in the mango orchard demonstrated that fruit set is generally enhanced in time asthe fruit development process advances from anthesis to physiological maturity. This is evident from the marked difference shown in the second production cycle (Fig 2). During the 2011-2012 cycle legume associations did not increase fruit set. The best scenario occurred in the C. spectabilis association with one fruit per panicle. The majority of associations showed increased fruit set during the initial days

40 35

10.00

30 8.00

C. longirostrata C. cajan V. unguiculata

6.00

No cover crop C. spectabilis

20 15

4.00

Temperature in °C

Number of fruits set per panicle

12.00

10 2.00

5 0

0.00

Days after anthesis (DAA)

Fig 1 Floral sex ratio in Ataulfo mango in association with bushy legumes (Fabaceae) during two growth cycles

Fig 2 Fruit set in bushy legume / Ataulfo mango associations during the 2012-2013 reproductive cycle

Production In mango/bushy legume associations, increased mango production (kg per tree) was observed in both cycles (2011-2012 and 2012-2013). During the first cycle, highest production was shown by C. spectabilis (22 kg) and C. longirostrata (21 kg) associations, as opposed to the untreated control which produced 5 kg per tree. During the second production cycle, C. longirostrata and C. spectabilis associations again showed higher yields of 55 and 36 kg per tree versus 24 kg per tree obtained in the control treatment. During the first cycle mango production (kg ha-1) was highest in the C. spectabilis and C. longirostrataassociations having obtained 562 and 530 kg ha-1 respectively. Second cycle results are more

indicative of the positive influence of bushy legumes on fruit yield (kg ha-1). C. spectabilis and C. longirostratafollowed the same performance pattern, resulting in higher yields of 924 and 1388 kg ha-1. Nubbin production showed a definite decrease in response to the presence of legumes (Fig 3) although this effect was not statistically analyzed. Behaviour of terminal meristems in mango is very complex. Five different bud types are produced and vegetative bud development from growth initiation to maturity lasts from 3 to 6 weeks, depending on the cultivar and on climatic conditions (Davenport and Nuñez-Elisea 1997). Knowledge of phenological stages allows definition of the precise moment at which floral development is useful for inflorescence

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Bushy Legumes Affects Reproductive Biology and Enhances Productivity in Mango manipulation. According to Ramírez and Davenport (2010), under tropical conditions, mango inflorescence occurs in response to the age of the latest vegetative flush whereas in subtropical environments, flowering is induced by low temperatures. Furthermore, Reece et al. (1949), state that there are mechanisms which control morphogenetic development of mango meristems and that floral expression is determined mainly by low temperatures and moisture stress. Temperature is important in regulating cellular division mechanisms. Sergent (1999) mentions that in perennial crops, factors such as radiation, rainfall and temperature affect flowering and fruit quality. Sergent (1999) and Reece et al. (1949) establish that flowering is induced by tree stress caused by biotic and abiotic factors, as is the case of sinthesis and accumulation of inductive substances which are synthesized under stress conditions produced by low temperatutres. Other authors, (León 1998, Lee et al. 2006), have shown that in the Soconusco region of Chiapas, Mexico, the flowering period is very heterogeneous and occurs from November to May. During this period one to three floral flushes occur depending on the climatic conditions of each cycle, mainly rainfall and photoperiod. Differences in the abundance of floral panicles in the two cycles observed coincided with the microclimatic changes recorded in the legume/mango associations. The authors suggest that these micro atmospheric changes are the result of environmental modifications of the microclimate due to the presence of the legumes which evidently reduce peaks in temperature and relative humidity in the mango philosphere and incorporate N fixed into the rhyzosphere through the legume/rhyzobium complex, improved soil moisture content and incorporated organic matter into the soil, all of which favoured panicle production and productivity. Of special importance is the fact that the C. longirostrata and C. spectabilis speciesproduced the highest dry biomass (259.01 and 257.47 kg/tree), which, incorporated into the soil, may have caused enhancement of the abundance of floral panicles in the mango associate. Similar results were reported by Lazaro (1988) who states that in most cases the effects of legume associations do not become evident during the first year, and furthermore, there are variations in the green biomass effects which persevere during the following 2 to 4 years. Sukhvibul et al. (2000) found, in research carried out in mango that floral panicle development occurs in trees which were maintained at temperatures between 0 and 30°C. They furthermore report that high temperatures increase panicle size although the Indian Horticulture Journal 5(3/4)

average number of flowers per panicle is reduced (413.3). Exposure of trees to low temperatures of 10 to 20°C increased the number of flowers (619.6). The percentage of hermaphroditic flowers decreased in poliembryonic cultivars and increased in monoembryonic varieties. Joubert et al. (1993) states that there are biotic factors such as scion, foliage orientation and tree age which can affect the number of hermaphroditic and masculine flowers. Furthermore, Gehrke et al. (2011) states that the reduction in the perfect flower ratio is more notorious in tropical polyembryonic cultivars. Singh (1969) establishes that there is a close association between high temperatures and increases in percent of hermaphroditic flowers. Among mangoes Ataulfo is characterized by having a high ratio of masculine to hermaphroditic flowers, there being factors which influence this process, such as high environmental temperatures, soil moisture and rainfall (Rodriguez 1998). (Bakula and Morín 1967, Avilán et al. 1998), establish that hermaphroditic flower ratios are affected by environmental, agronomic and genetic factors and Schafferet et al. (1994) mention that sex of newly blooming flowers is affected by the levels of light received. Hence, buds exposed to direct sunlight are more precocious and form a greater number of hermaphrodite flowers than those under shade. The increase in perfect flowers is related to temperature during morphogenesis of flowers exposed to greater sunlight.

Fig 3 Ataulfo mango fruit production in mango/legume associations during two crop cycles (2011-2012 and 2012-2013)

Recent research has demonstrated that flower and fruit abortion in mango is due mainly the formation of abscicion layers and to other factors such as rainfall, humidity and temperature (Young 1987). Gehrke 67

Francisco et al. 2015 (2008) refers to Ataulfo mango and states that the ratio of flowers emitted to set fruits is approximately 3000:1 with an average set of 4 to 5 fruits per panicle under normal conditions and in extreme cases there are less than 0.01 fruits set per floral panicle. Barrera (2011) established that fruit abortion can occur up to 75 days after anthesis. Litz (1997) states that total loss of set fruits are more common during the first days after anthesis than upon reaching apparent physiological ripeness. Rodriguez (1989) states that the main fruit drop occurs when fruits are in the “mustard seed” and “pea” size. Magness and Traub (1941) mention that fruit formation is influenced mainly by insolation and light intensity and Tabuenca (1965) states that in stone fruits soil humidity is good for proper fruit production. Results obtained in the different treatments, especially during the second production cycle, are presumably due to the accumulation of reserves in the trees which appears to improve production in addition to increasing nutrient supply, especially of nitrogen supplied by the legumes. These plants establish a symbiotic association with nitrogen-fixing microorganisms of the Rhizobium genera in the soil which are in turn in a symbiotic relationship with mycorhyzic fungi allowing the fixing of atmospheric nitrogen and consequently enhancing water absorption and soil nutrient assimilation. Results indicate that by associating bushy legumes in mango plantations, yields are improved in the second year. This is probably due to the decomposing of organic matter and consequent supply of available nutrients to the

mango trees. It should be noted that during the first production cycle, organic matter supplied by the legumes was not fully decomposed and hence there was no difference in soil fertility in the different treatments. This is supported by Lazaro (1998) who mentions that legume association effects are not visible until after 2 to 4 years. Studies on biological N fixation by legumes in corn have shown a high rate of nitrogen fixation which satisfies N requirements, in addition to presenting other advantages such as weed control, soil erosion protection and other ecological benefits. Upon analysis of the differences obtained in the present study, it is concluded that these are due primarily to the use of reserves stored in the mango trees, in addition to temperature and moisture stabilization of the microclimate and to fertility improvement resulting from the association with legume crops. Yield improvement obtained from the legumes is expressed after some time, this being due to the fact that in agroecological systems, stability is obtained after three or four years. According to Gehrke (2008) yields in Ataulfo mango orchards in the Soconusco region of Mexico are below four tons ha-1 and some orchards produce no commercial quality mangoes at all. Yields have been decreasing year by year. Nubbin production showed a definite reduction and it is suggested that this is due to the micro environment changes which resulted in more efficient cross pollination of the Ataulfo mango and to decreased temperatures.

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