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Fluctuation in Abundance of Adult Fruit Flies 1 at

Rosamorada and San Blas, Nayarit, México


Authors: Isiordia-Aquino, Néstor, Robles-Bermúdez, Agustín,
Cambero-Campos, Octavio J., Santillán-Ortega, Candelario, Jiménez-
Meza, Víctor M., et al.
Source: Southwestern Entomologist, 42(3) : 731-744
Published By: Society of Southwestern Entomologists
URL: https://doi.org/10.3958/059.042.0312

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VOL. 42, NO. 3 SOUTHWESTERN ENTOMOLOGIST SEP. 2017

Fluctuation in Abundance of Adult Fruit Flies1 at Rosamorada and San Blas,


Nayarit, México

Fluctuación en Abundancia de Moscas de la Fruta Adultas1 en Rosamorada y


San Blas, Nayarit, México

Néstor Isiordia-Aquino2, Agustín Robles-Bermúdez2, Octavio J. Cambero-Campos2,


Candelario Santillán-Ortega3, Víctor M. Jiménez-Meza2, and
Ricardo J. Flores-Canales2

Abstract. The economy of Nayarit depends on fruit, especially mango, Mangifera


indica L., and citrus. However commercialization of fruit is affected by abundant
fruit flies (Diptera: Tephritidae). To know the diversity of Anastrepha Schiner and
determine its population dynamics on species in marginal areas of the municipalities
of Rosamorada and San Blas, between January and December 2011, 128 McPhail
traps baited with hydrolyzed protein were prepared each week. Fruit flies captured
were preserved in 70% ethanol and sorted by sex and species according to an FTD
index of numbers of flies trapped per day. Of 563 specimens collected, 442
(78.51%) were from Rosamorada and 121 (21.49%) at San Blas, with a male:
female sex ratio of 1:1.9 and 1:1.6, respectively, at each municipality. At
Rosamorada (FTD 0.143), species identified were Anastrepha ludens (Loew) (210:
47.51%), A. striata Schiner (114: 25.79%), and A. obliqua (Macquart) (113:
25.57%), captured 70.2, 81.0 and 51.3% of the time, respectively, while A. sp. (3:
0.68%) and A. serpentina (2: 0.45%) occurred only rarely (2.7 and 8.1%,
respectively). At San Blas (FTD 0.0111), A. obliqua (57: 47.11%) and A. striata (57:
47.11%) were captured 70.3 and 62.9% of the time, respectively; A. ludens (6:
4.96%) was found less commonly (14.8%), and A. sp. (1: 0.82%) was found rarely
(3.7%). Most fruit flies were trapped between February and August, coinciding with
the fruiting period, with no apparent effect of abiotic factors such as temperature or
precipitation on abundance.

Resumen. Nayarit sustenta su economía en especies frutales como mango,


Mangifera indica L., y cítricos principalmente; sin embargo, su comercialización es
afectada por la alta incidencia del complejo moscas de la fruta (Díptera:
Tephritidae). Con el propósito de conocer la diversidad de especies de Anastrepha
Schiner y determinar su dinámica poblacional sobre especies establecidas en
áreas marginales de los municipios de Rosamorada y San Blas, entre Enero y
Diciembre de 2011 se realizaron trampeos semanales con 128 trampas McPhail
cebadas con proteína hidrolizada; los especímenes capturados se conservaron en
________________________
1
Diptera: Tephritidae
2
Unidad Académica de Agricultura, Universidad Autónoma de Nayarit. Km 9 Carretera Tepic-
Compostela, CP 63780 Xalisco, Nayarit.
3
Departamento de Parasitología Agrícola, Universidad Autónoma Chapingo. Km 38.5 Carretera
México-Texcoco, CP 56230 Chapingo, Estado de México.

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alcohol (70%) y se agruparon por sexo y especie, conforme al índice MTD. De 563
especímenes recolectados, 442 (78.51%) correspondieron a Rosamorada y 121
(21.49%) a San Blas, con una proporción sexual de machos contra hembras de
1:1.9 y de 1:1.6, respectivamente, para cada municipio; en Rosamorada (MTD
0.0143), las especies identificadas fueron Anastrepha ludens (Loew) (210: 47.51%),
A. striata Schiner (114: 25.79%), y A. obliqua (Macquart) (113: 25.57%), ubicadas
como constantes (70.2, 81.0, y 51.3%, respectivamente), mientras que A. sp. (3:
0.68%) y A. serpentina (2: 0.45%), resultaron en ocurrencia rara (2.7 y 8.1%,
respectivamente); en San Blas (MTD 0.0111), las especies identificadas fueron A.
obliqua (57: 47.11%) y A. striata (57: 47.11%), ubicadas como constantes (70.3 y
62.9%, respectivamente), A. ludens (6: 4.96%), de ocurrencia común (14.8%), y A.
sp. (1: 0.82%), de ocurrencia rara (3.7%). Las mayores capturas ocurrieron entre
febrero y agosto, coincidiendo con el periodo de fructificación, sin efecto aparente
de factores abióticos como temperatura y precipitación sobre las poblaciones.

Introduction

Internationally, Mexico has several competitive advantages in food


production compared to other countries; its diversity of climates and environmental
conditions that favor productive potential allows a wide range of products to be
produced at different times of the year. Its geographical location,
commercialization, and strict phytosanitary and safety standards favor production,
which is reflected in much commercialization with international markets. Fruit and
vegetable production in Mexico is a major agricultural activity, with important fruit
species such as mango (Mangifera indica L.), lemon (Citrus limon (L.), banana
Musa paradisiaca (L.), apple (Pyrus malus L.), peach (Prunus persica L.), pineapple
(Ananas comosus (L.) Merr.), grapefruit (Citrus paradisi Macf.), and papaya (Carica
papaya L.) grown on approximately 22.2 million hectares (SAGARPA-SIAP 2015).
The social importance is in the amount of labor required during the production
process, in collection of foreign money, and in the impact on nutrition of Mexican
consumers.
Plant health is an important and determining factor in trade of fresh products
between countries and regions. Fruit flies (Diptera: Tephritidae) threaten
commercial quality of horticultural products (FAO 2008). In Mexico, the presence
and incidence of fruit flies is a quarantine barrier for export of fruits, which is a
serious problem because all areas with fruit production have diverse host plants and
agroclimatic conditions favorable for establishment and propagation of fruit flies.
Produce is destroyed in the field by attack from several species of Anastrepha
Schiner, registered as economically important, that directly and indirectly affect
production and commercialization worldwide (Uchoa and Nicacio 2010).
Knowledge of biological aspects of species in an area provides an advantage
in implementation of appropriate technologies to establish integrated management
strategies. At municipalities such as Rosamorada and San Blas at Nayarit are
favorable agroecological conditions for proliferation of native and introduced species
of fruit flies that damage the economy of producers of the region because
taxonomic and ecological knowledge of each fruit hunger species and its
geographical distribution in marginal areas is of transcendental importance (NOM-
023-FITO-1995 1999). Likewise, farmers need knowledge of the life cycle and
abundance of pests and their natural enemies, as well as the influence of weather
conditions such as temperature, humidity, and precipitation to make accurate and

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timely decisions (Coscollá 1980), which together with knowledge of the diversity of
species in an area are the first steps to design studies aimed at establishing
appropriate technologies for management of insect species (Castañeda et al. 2010).
The present work aimed to identify species of fruit flies (Anastrepha) and determine
their population dynamics in marginal areas in the study area.

Materials and Methods

The study was at the municipalities of Rosamorada and San Blas in the
north-central region of the state of Nayarit. The first municipality is between
parallels 21º56' and 22º22' N latitude and meridians 104º55' and 105º35' W
longitude in the northern part of the state, at altitudes between 0 and 1,300 m above
sea level, with average annual temperatures of 22-28oC and precipitation from
1,100-2,200 mm, with a warm subhumid climate with summer rains
(seplan.gob.mx/des/pdms/pdm_ros.pdf), and mangrove (Laguncularia racemosa
(L.) C.F. Gaerth.) vegetation, thorny scrub, halophytic vegetation, and secondary
subcaducifolia secondary forest (http://sinat.semarnat.gob.mx/dgiraDocs/
documentos/nay/estudios/2008/18NA2008HD029.pdf). The municipality of San
Blas is on the central coast between parallels 21º20' and 21º45' N latitude and
meridians 105º01' and 105º28' W longitude, with altitude 0 to 1,200 m above sea
level, average annual temperature of 25.6oC, average annual rainfall of 1,316.3
mm, and a warm-humid climate with rainfall from June to October
(seplan.gob.mx/des/pdms/pdm_san.pdf). The vegetation includes subcaducifolia
median forest, pine forest, low deciduous forest, pine-oak forest, Encino, and
mangrove forest being the dominant vegetation (http://digaohm.semar.gob.mx/
cuestionarios/cnarioSanblas.pdf).
Population dynamics of fruit flies of the genus Anastrepha in some species of
fruit in marginal (non-commercial) areas were determined from January to
December 2011. McPhail glass traps containing a bait mixture of commercial
hydrolyzed protein and 5 g of borax (sodium borate pentahydrate) diluted in 250 ml
of water were used to capture adults (NOM-023-FITO-1995 1999, Tucuch-Cauich et
al. 2008). Once the host trees were selected on several trapping routes at the two
municipalities, 128 traps were placed (92 at Rosamorada and 36 at San Blas)
according to placement, inspection, and receipt procedure of the Instituto
Colombiano Agropecuario (ICA 2005). Several fruit species at both municipalities
were considered, with rotations of traps according to the availability of food (fruit) for
the insect, during the phenological period from fruiting through harvest of some
species of fruit listed in the Official Mexican Standard, NOM-023 Fito-1995, such as
mango (M. indica L.: Anacardiaceae), yellow plum (Spondias mombin L.:
Anacardiaceae), red plum (Spondias sp.: Anacardiaceae), guava (Psidium guajava
L.: Myrtaceae), arrayan (Psidium sartorianum (Berg) Nied: Myrtaceae), sweet
orange (Citrus sinensis (L.) Osbeck: Rutaceae), bitter orange (C. aurantium L.:
Rutaceae), sweet lime (C. limetta Risso: Rutaceae), tangerine (C. reticulata Blanco:
Rutaceae), and white sapote (Casimiroa edulis Llave et lok: Sapotaceae).
To measure the species richness of the genus Anastrepha, adult specimens
collected each week in traps at both municipalities were rinsed with tap water and
deposited in 70% ethanol for preservation in 40-ml plastic vials (one per trap). The
insects were transferred to the fruit fly taxonomy laboratory of the State Committee
of Plant Protection at Nayarit to separate by sex and identify by comparison with
preserved specimens, for which a stereoscopic microscope and dichotomous keys

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and criteria by Steyskal (1977), Hernández-Ortíz (1992), and SENASICA-DMF
(2010) were used.
Weather data at Rosamorada and Las Palmas were obtained from
meteorological stations operated by the Santiago Ixcuintla Experimental Station of
the National Institute of Forestry, Agriculture and Livestock Research (CESIX-
INIFAP) in the study area at both municipalities. Data on maximum and minimum
temperatures, relative humidity, and rainfall were averaged by month (Table 1).
To determine the abundance of fruit flies each week, the number of flies
caught per trap per day (FTD) (Triguero 2005, FAO 2008) was used for each of the

months and municipalities, according to the formula:  ൌ ୘‫כ‬ୈ, where, F = total
number of flies collected, T = number of traps, and D = days of exposure of traps in
the field. After the flies were counted, a grouping of the monthly averages of the
species, expressed as flies per trap per day, and weather data at each municipality
were correlated using the Pearson coefficient test.
Constancy or occurrence of each species was verified at the two
municipalities by using the constancy index of Sampaio et al. used by Nolasco and
Lannacone (2008), where the species were constants (C) when recorded during
more than 50% of the weeks, common (c) when present between 10 and 50% of
the weeks, and rare (r) when present during 10% or fewer of the weeks. To
measure the specific biodiversity at the study area, the Shannon Index (Moreno
2001, Pla 2006) was used, according to the formula: H´ = -Ʃsi=1 (pi) (log2pi), where
S = number of species (richness), pi = proportion of individuals of species i in
௡௜
respect to the total number of individuals (relative abundance of species i): ே , ni =
number of individuals of species i, and N = number of all individuals of all species.

Table 1. Weather Data Recorded in 2011 at the Municipalities of Rosamorada and


San Blas, Nayarit
Rosamarada Municipality San Blas Municipality
Month T. max T. min Humidity Rain T. max. T. min. Humidity Rain
January 23.97 11.10 88.00 0.40 28.18 12.89 92.03 0.20
February 29.27 9.57 84.00 0 28.46 12.35 90.00 0
March 32.18 11.95 85.25 0 30.36 14.10 89.42 0
April 28.92 13.96 77.50 0 31.90 15.85 84.63 0
May 30.13 19.12 78.00 0 33.10 19.00 82.48 0.20
June 34.92 23.96 79.40 14.40 32.95 22.70 86.40 157.20
July 33.13 23.83 87.29 128.00 31.44 22.24 96.16 523.40
August 33.47 24.15 88.14 325.80 32.38 22.58 95.81 632.20
September 33.86 23.89 94.12 119.00 32.53 23.07 95.57 331.60
October 34.47 22.76 93.93 5.60 32.84 22.59 93.10 36.80
November 33.58 16.53 95.30 0 31.62 18.82 89.40 0
December 29.01 12.45 95.03 0 27.70 14.83 92.87 0
Total 31.40 17.77 91.10 593.20 31.12 18.41 90.68 1681.60
T. max. = maximum temperature (oC); T. min. = minimum temperature (oC);
Humidity = relative humidity (%); Rain = rainfall (mm)

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Results

Diversity of Anastrepha Species. During the study period, 5,960 traps


were inspected: 4,409 (73.98%) at Rosamorada and 1,551 (26.02%) at San Blas,
with 563 adult specimens of Anastrepha, of which 442 (78.51%) were from
Rosamorada and 121 (21.49%) from San Blas (Table 2). Of the total number of
captures at the municipality of Rosamorada, five species were identified, with
decreasing dominance of A. ludens (Loew) (210: 47.51%), followed by A. striata
Schiner (114: 25.79%), A. obliqua (Macquart) (113: 25.57%), A. sp. (3: 0.68%), and
A. serpentina (Wiedemann) (2: 0.45%). The four species captured at San Blas
were in descending order A. obliqua (57: 47.11%), A. striata (57: 47.11%), A. ludens
(6: 5.0%, and A. sp. (1: 0.83%).
With a global index of 0.0143 at Rosamorada, the largest monthly FTD
values of 0.0431, 0.0305, and 0.0270 were recorded in May, July, and June,
respectively, while the smallest in November, October, and December, with 0.0006,
0.0007, and 0.0009, respectively. At San Blas, average similar numbers to those at
Rosamorada were recorded, with an annual index of 0.0111, where the largest
values of 0.0501, 0.0366, and 0.0164 were obtained in February, April, and July
respectively, and the least in November, October, and December, with 0.0007,
0.0009, and 0.0013, respectively (Table 2).
Separation of adults by sex (Table 3) showed that of the total number of fruit
flies caught at the municipality of Rosamorada, 293 (66.29%) were females (♀) and
149 (33.71%) were males ( ), with a male : female sex ratio of 1:1.9 for all species,
while the proportion for each species was 1:1.8 for A. ludens (75 males and 135
females), 1:1.6 for A. striata (43 males and 71 females), 1:2.9 for A. obliqua (29
males and 84 females), 1:2 for A. sp. (one male and two females), and 1:1 for A.
serpentina (one male and one female). At the municipality of San Blas, 76
(62.81%) were females and 45 (37.19%) males, with a male:female sex ratio of
1:1.6 (Table 4). The sex ratio was 1:1.8 for A. obliqua (20 males and 37 females),
1:1.3 for A. striata (24 males and 33 females), and none for A. ludens (no male and
six females) or A. sp. (no male or female).
Population Fluctuation of Anastrepha Species. At Rosamorada, A.
ludens was most abundant in February (48), June (40), and July (34), and least in
January, September, October, and November (none caught); A. obliqua was most
abundant in June (39), August (29), and June (26), with none caught in January,
February, April, October, November, or December; A. striata was most abundant in
June (25), February (23), and March (23), and least in April (one), December (one),
October (two), and November (two); A. serpentina was caught only in July (two),
while three A. sp. adults were caught in June. At the municipality of San Blas,
fewest A. ludens were trapped in April (three), March (two), and May (one); A.
obliqua was most abundant in August (19), July (16), and June (nine), with none
caught in January, February, November, or December; most A. striata occurred in
March (16), February (13), and April (13); few in April (one), November (one), and
December (one), and none in October; and only one A. sp. was recorded in July.
At the municipality level at Rosamorada, the species A. ludens, A. obliqua,
and A. striata were constant (C) at 70.2, 51.3, and 81.0%, respectively, with rare (r)
collection of A. serpentina and A. sp. at 2.7 and 8.1%, respectively (Table 5). At
San Blas, A. obliqua and A. striata were constant (70.3 and 62.9%, respectively), A.
ludens was common (c) at 14.8%, while A. sp. was rare (3.7%). The specific
biodiversity was dominant (d) for A. ludens at Rosamorada and A. obliqua and A.

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Table 2. Anastrepha Species Captured in McPhail Traps on Marginal Areas of Rosamorada and San Blas, Nayarit
Rosamorada Municipality San Blas Municipality
A. A. A. A. A. A. A. A. A.
Month Reviewed ludens obliqua striata serpentina sp. Total FTDa Reviewed ludens obliqua striata sp. Total FTDa
January 239 0 0 3 0 0 3 0.0017 111 0 0 3 0 3 0.0030
February 384 48 0 23 0 0 71 0.0264 37 0 0 13 0 13 0.0501
March 480 19 2 23 0 0 44 0.0130 184 2 1 16 0 19 0.0148
April 288 22 0 1 0 0 23 0.0114 74 3 3 13 0 19 0.0366
May 192 32 11 15 0 0 58 0.0431 36 1 1 2 0 4 0.0158
June 480 40 26 25 0 3 94 0.0270 185 0 9 5 0 14 0.0108
July 370 34 39 4 2 0 79 0.0305 148 0 16 0 1 17 0.0164

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August 480 14 29 10 0 0 53 0.0157 185 0 19 1 0 20 0.0154
September 384 0 6 5 0 0 11 0.0040 148 0 7 2 0 9 0.0087
October 384 0 0 2 0 0 2 0.0007 147 0 1 0 0 1 0.0009
November 440 0 0 2 0 0 2 0.0006 185 0 0 1 0 1 0.0007
December 288 1 0 1 0 0 2 0.0009 111 0 0 1 0 1 0.0013
Total 4409 210 113 114 2 3 442 0.0143 1551 6 57 57 1 121 0.0111

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a
FTD = number of fruit flies per trap per day

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Table 3. Numbers and Sex Ratio of Anastrepha Species Captured in McPhail Traps at Rosamorada, Nayarit
A. ludens A. obliqua A. striata A. serpentina A. sp. Total flies
Month st ♀ ♂ p/s st ♀ ♂ p/s st ♀ ♂ p/s st ♀ ♂ p/s st ♀ ♂ p/s total ♀ ♂ p/s
January 0 0 0 0 0 0 0 0 3 2 1 1:2 0 0 0 0 0 0 0 0 3 2 1 1:2
February 48 29 19 1:1.5 0 0 0 0 23 14 9 1:1.5 0 0 0 0 0 0 0 0 71 43 28 1:1.5
March 19 12 7 1:1.7 2 2 0 0 23 15 8 1:1.8 0 0 0 0 0 0 0 0 44 29 15 1:1.9
April 22 10 12 1:0.8 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 23 11 12 1:0.9

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May 32 19 13 1:1.4 11 8 3 1:2.6 15 10 5 1:2 0 0 0 0 0 0 0 0 58 37 21 1:1.7
June 40 31 9 1:3.4 26 20 6 1:3.3 25 14 11 1:1.2 0 0 0 0 3 2 1 1:2 94 67 27 1:2.4
July 34 24 10 1:2.4 39 30 9 1:3.3 4 3 1 1:3 2 1 1 1:1 0 0 0 0 79 58 21 1:2.7
August 14 9 5 1:1.8 29 20 9 1:2.2 10 6 4 1:1.5 0 0 0 0 0 0 0 0 53 35 18 1:1.9
September 0 0 0 0 6 4 2 1:2 5 3 2 1:1.5 0 0 0 0 0 0 0 0 11 7 4 1:1.7
October 0 0 0 0 0 0 0 0 2 1 1 1:1 0 0 0 0 0 0 0 0 2 1 1 1:1
November 0 0 0 0 0 0 0 0 2 1 1 1:1 0 0 0 0 0 0 0 0 2 1 1 1:1

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December 1 1 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 2 2 0 0
Total 210 135 75 1:1.8 113 84 29 1:2.9 114 71 43 1:1.6 2 1 1 1:1 3 2 1 1:2 442 293 149 1:1.9

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st = subtotal; ♀ = females; ♂ = males; p/s = sex ratio between males and females
Table 4. Numbers and Sex Ratio of Anastrepha Species Caught in McPhail Traps
at San Blas, Nayarit
A. ludens A. obliqua A. striata A. sp. Total flies
Month st ♀ ♂ p/s st ♀ ♂ p/s st ♀ ♂ p/s st ♀ ♂ p/s total ♀ ♂ p/s
January 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 3 3 0 0
February 0 0 0 0 0 0 0 0 13 6 7 1:0.8 0 0 0 0 13 6 7 1:0.8
March 2 2 0 0 1 1 0 0 16 9 7 1:1.2 0 0 0 0 19 12 7 1:1.7
April 3 3 0 0 3 2 1 1:2 13 8 5 1:1.6 0 0 0 0 19 13 6 1:2.1
May 1 1 0 0 1 1 0 0 2 2 0 0 0 0 0 0 4 4 0 0
June 0 0 0 0 9 4 5 1:0.8 5 3 2 1:1.5 0 0 0 0 14 7 7 1:1
July 0 0 0 0 16 10 6 1:1.6 0 0 0 0 1 0 1 0 17 10 7 1:1.4
August 0 0 0 0 19 14 5 1:2.8 1 1 0 0 0 0 0 0 20 15 5 1:3
September 0 0 0 0 7 5 2 1:2.5 2 1 1 1:1 0 0 0 0 9 6 3 1:2
October 0 0 0 0 1 0 1 0 0 0 0 0 0 0 0 0 1 0 1 0
November 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 1 0 1 0
December 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 1 0 1 0
Total 6 6 0 0 57 37 20 1:1.8 57 33 24 1:1.3 1 0 1 0 121 76 45 1:1.6
st = subtotal; ♀ = females; ♂ = males; p/s = sex ratio between males and females

striata at both municipalities and was not dominant (n) for A. ludens at San Blas or
A. serpentine and A. sp. at both municipalities. The Shannon Index (H') was 1.10
for Rosamorada and 0.89 for San Blas, represented by a wealth of five and four
species, respectively.
In relation to the Pearson correlation coefficients (CC) (Table 6), when the
average catches of each species, expressed in monthly FTD, were compared with
temperature (maximum and minimum), relative humidity, and rainfall recorded
monthly at Rosamorada, for A. ludens, as the relative humidity increased, the value
of FTD decreased (CC -0.60960; PR 0.0353), similar to what happened with A.
striata (CC -0.59882; PR 0.0397); for A. obliqua, as the minimum temperature
decreased, FTD increased (CC 0.66602; PR 0.181); for A. serpentina and A. sp.,
minimum temperature, relative humidity, and precipitation were not correlated with
FTD. At San Blas, with A. ludens, there was negative correlation between FTD and
relative humidity (CC -0.74116; PR 0.0050) as the relative humidity increased, FTD
decreased; for A. obliqua, as the minimum temperature increased, the FTD
increased (CC 0.65310; PR 0.0213), with an inverse effect on A. striata, where, as
the minimum temperature increased, the FTD decreased (CC -0.60209; PR
0.0383); for A. sp., minimum temperature, relative humidity, and precipitation did not
affect the FTD.

Discussion

Adults of the different species of Anastrepha fluctuated in abundance at both


municipalities during all months of the year. A different seasonal occurrence of
fluctuation in abundance occurred at each municipality, similar to what happened for
A. obliqua at Maracay, Venezuela (Boscán de Martínez and Godoy 1986), A.
serpentina at Aragua, Venezuela (Boscán de Martínez and Godoy 1987), and
Ceratitis capitata (Wied.) throughout the year because of fruit available throughout
the breeding season of the species at Buenos Aires, Argentina (Segura et al. 2004)
and at Montenegro (Radonjic et al. 2013).

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Table 5. Faunal Analysis of Anastrepha Species Collected in 2011 by McPhail Traps in Marginal Areas of Rosamorada and
San Blas, Nayarit
Anastrepha Rosamorada Municipality San Blas Municipality
species ni Frequency (%) Dominance %O pi H´ ni Frequency(%) Dominance %O pi H´
A. ludens 210 47.51 d 70.2C 0.4751 -0.3535 6 4.96 n 14.8c 0.0496 -0.1489
A. obliqua 113 25.57 d 51.3C 0.2557 -0.3487 57 47.11 d 70.3C 0.4711 -0.3545
A. striata 114 25.79 d 81.0C 0.2579 -0.3495 57 47.11 d 62.9C 0.4711 -0.3545
A. serpentina 2 0.45 n 2.7r 0.0045 -0.0243 0 0 n 0r 0 0
A. sp. 3 0.68 n 8.1r 0.0068 -0.0339 1 0.82 n 3.7r 0.008 -0.0393
Total number of
442 1.1099 121 0.8972
individuals (N)
ni = number of individual of species i; dominance: d (dominant), n (nondominant); %O = occurrence percentage: C = constant, c =
common, r = rare
H´(Shannon-Weaver Index): H´ = -Ʃsi = 1 (pi) (log2pi); pi = relative abundance of species i (pi = ni/N)

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Table 6. Correlation Coefficient between Weather Data and FTD of Anastrepha spp. at Rosamorada and San Blas, Nayarit
Rosamorada Municipality San Blas Municipality
Maximum Minimum Relative Maximum Minimum Relative
Species temperature temperature humidity Rainfall temperature temperature humidity Rainfall
-0.068041 -0.021431 -0.609601 -0.129871 0.267281 -0.21411 -0.741161 -0.325751
A. ludens

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0.83362 0.94732 0.03532* 0.68752 0.40102 0.50402 0.00502* 0.30152
0.368961 0.666021 0.092951 0.547771 0.484001 0.65311 0.356631 0.359221
A. obliqua
0.23792 0.01812* 0.91502 0.06522 0.11092 0.02132* 0.25522 0.25102

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1 1 1 1 1 1 1
0.00492 -0.09297 -0.59882 -0.17239 -0.34839 -0.60209 0.36060 -0.359091
A. striata 2 2 2 2 2 2 2
0.9879 0.7738 0.0397 * 0.5921 0.2671 0.0383 * 0.2495 0.25172
1 1 1 1
0.16854 0.32897 0.10603 0.25016
A. serpentina
0.600502 0.296402 0.742902 0.432902
1 1 1
0.34386 0.33603 -0.16224 -0.111551 0.508501 0.285621 0.387451 0.528371
A. sp. 2 2 2 2 2 2 2
0.27380 0.28560 0.61440 0.73000 0.87530 0.3682 0.2134 0.077402
1
Correlation coefficient; 2Prob > |R|; *The variables were correlated (α = 0.05)
The fruiting periods of the different kinds of fruit alternated throughout the
breeding season of the flies, assuring an almost uninterrupted supply of resources.
At Rosamorada, A. ludens adults were caught from early February to late August
and in December, with peaks in February, June, and July, coinciding with the
availability of fruiting stage citrus and mangoes, both native and commercial, and
the period of more rainfall, similar to that reported by Tucuch-Cahuich (2008) for
mango at Campeche. Aluja (1993) asserted that adult fruit flies in commercial
orchards had different fluctuations in abundance from year to year, possibly
because of host availability and weather, mainly rain. A. obliqua was detected in
March and from May to September, with the maximum number caught from June to
August, coinciding with availability of mango fruit, its natural host, similar to that
reported by Aluja et al. (1996). A. striata was found in all months, with greater
incidence in February-March and May-June, coinciding with the availability of
arrayan and guava fruits. A. serpentina (two) and A. sp. (three) were caught only in
July and June, respectively. At San Blas, despite adults present throughout the
year, in general most were caught in February-April and June-August; unlike at
Rosamorada where it was the dominant species, A. ludens (six) were first recorded
in March-May because of the presence of citrus in the fruiting stage. A. obliqua
were all caught between March and October, with most between July and August
because of red and yellow plums as well as native and commercial mangoes,
similar to reports by Celedonio-Hurtado et al. (1995), Aluja et al. (1996), and
Martínez et al. (2007). A. striata occurred during 10 months of the year, with the
peak in February-April because of availability of guava fruit, with a single A. sp. in
July, and no A. serpentina caught. Fluctuation in abundance of A. obliqua was
similar to that reported by Boscán de Martínez and Godoy (1986) who found no
relation to temperature or precipitation, but coinciding with the harvest season of
mango. The peak in abundance at the end of the mango harvest coincided with
that in guava (Triguero 2005).
Compared with weather factors, fruit availability was the most determining
factor in variation in abundance of fruit flies of the genus Anastrepha (Jiron and
Hedstrom 1991, Aluja 1994, Uramoto 2002, Aluja and Birke 2014). Fluctuation in
abundance of the insect varied according to the season, location, and availability of
fruit (Triguero 2005, González et al. 2011), with the presence of alternative host and
weather conditions, especially temperature and precipitation being the fundamental
factors affecting fluctuations in abundance (Aluja 1994).
In relation to the FTD index during the period, with the exception of the
months with the greatest incidence of fruit flies at Rosamorada, with 0.0431 (May),
0.0305 (June), and 0.0270 (July), and at San Blas, with 0.0501 (February) and
0.0366 (April), within the phytosanitary category under phytosanitary control, fruit
flies during most months at both municipalities were within the phytosanitary
category of low prevalence of fruit flies, with indices ≤0.100 for at least 6 months
(NOM-023-FITO-1995 1999).
In general, precipitation did not affect the FTD of any of the four fruit fly
species according to Montoya et al. (2008) who indicated that the factor did not
have a significant impact on emergence and survival of adults, and that their annual
fluctuation in abundance was correlated with factors such as the fruiting phenology
of hosts. At Rosamorada, the FTD value (CC -0.60960; PR 0.0353) for A. ludens
decreased as relative humidity increased similar to what happened with A. striata
(CC -0.59882, PR 0.0397), and with A. ludens at San Blas (CC -0.74116; PR
0.0050). The results differed from those by Aluja (1994) who stated that with dry

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conditions more fruit flies died, especially when soil was dry. Sequeira et al. (2001)
found that optimum humidity was 70-100%, contrary to what was recorded in our
study.
The sex ratio of males to females was 1:1.9. This coincided with previous
reports on McPhail trapping in Mexico (López and Becerril 1967, Houston 1981)
despite the use of yeast as hydrolyzed protein (Malo and Zapien 1994) and close to
1:1.7 at Ica and Piura (Peru). As a male ended the copulation process, it tried to
mate with other females (Nolasco and Lannacone 2008), while the female first
looked for nutrients required for reproduction and a suitable substrate for oviposition
(Aluja 1993).
For specific constancy or occurrence, Sampaio et al. (2002) found that A.
ludens (70.2%), A. obliqua (51.3%), and A. striata (81%) were constant, with rare
occurrence of A. serpentina (2.7%) and A. sp. (8.1%). At San Blas, A. ludens had
common occurrence (14.8%) and A. obliqua and A. striata were constant (70.3 and
62.9%, respectively), while A. sp. rarely occurred (3.7%). The results coincided with
that found for dominance of A. striata by Nolasco and Lannacone (2008) who in the
Department of Ica and Valle de Pisco (Peru) obtained occurrence of 57.3 (four
species) and 82.1% (three species), respectively. A. serpentina was less dominant
given its food specificity. At Rosamorada, the Shannon Index was 1.10 for five
species of fruit flies, identical to that obtained for eight species at Xanxere County,
Brazil (García et al. 2003), and close to that reported by Veloso et al. (1994), with
1.5 for 18 species. At San Blas, an index of 0.89 was obtained for four species,
close to the 0.75 obtained by Uramoto (2002) at Sao Paulo, Brazil.
In conclusion, fluctuation in abundance of different species of Anastrepha in
marginal areas depends on availability of fruit in the fruiting stage, with no apparent
effect of weather on each species. Control actions against the fly complex should
be started in January when the first adult is caught, which would avoid increasing
abundance favored by weather conditions and availability of various fruit as food
and to avoid the fruiting stage of commercial species such as mango and plum in
the region. Because numbers of fruit flies trapped per day were ≤0.10 during most
months of the year, the study area was within the phytosanitary status of a low pest
prevalence zone that can be maintained through integrated management with
sterile insect technique through inundative releases of sterile A. ludens and A.
obliqua playing a preponderant role.

Acknowledgment

To the State Committee of Plant Protection in Nayarit, for the facilities and
technical support provided for the study, by the immediate staff assigned to the
National Campaign against Fruit Flies.

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