Location and description of the study area

The Tezozómoc Cultural and Recreational Park (PCyRT) was designed in 1978 by the architect Mario Schjetman de Garduño, and opened on March 21, 1982 as a cultural-recreational space, in a densely populated area in the northwest of Mexico City, where there are few green areas. The purpose of this project was to recreate the topography-orography of the Valley of Mexico and its five lakes from the end of the 15^th century, to offer through an cultural tour an historical and ecological vision in an easy and attractive way (^{Reséndiz et al., 2015}).

The PCyRT is located northwest of the Azcapotzalco City Hall in Mexico City; its coordinates are 19°29’05” N and 99°12’38” West, at 2 250 meters above sea level (Figure 1). It covers an area of 270 000 m² (^{González and Moctezuma, 1999}-2000). It borders to the north with the Tlalnepantla municipality, to the west with the municipality Naucalpan, to the south with the Cuauhtémoc and Miguel Hidalgo mayoralties and to the East with that of Gustavo A. Madero.

Figure 1 Location of Tezozómoc Recreational and Cultural Park. 

According to the Azcapotzalco weather station, the climate corresponds to type C (w₀), subhumid temperate with rains in summer, of medium humidity, according to the Köeppen classification modified by García (^{Cuaderno Estadístico Delegacional, 2000}).

At present, the soils in the Tezozómoc Park are sanitary landfills composed mainly of rubble and various garbage materials, so given its anthropic influence this type of soil is known as Androsol.

The flora of the park is represented by the following species, some of which are present in other major urban parks such as San Juan de Aragón (^{González et al., 2014}): eucalyptus (Eucalytus globulus Labill.; E. camaldulensis Dehnh), ash (Fraxinus uhdei (Wenz.) Lingelsh), white poplar (Populus alba L.), jacaranda (Jacaranda mimosifolia D. Don), peach (Prunus persica (L.) Stokes), Mexican hawthorne (Crataegus mexicana DC.), avocado (Persea americana Mill.), Chinese orange blossom (Pittosporum tobira (Thunb.) A. T. Aiton), laurel rose (Nerium oleander L.), scarlet firethorn (Pyracantha coccinea M. Roem.), orchid tree (Bauhinia variegata L.), Montezumae cypress (Taxodium mucronatum Ten.), ahuejote (Salix bonplandiana Kunth), loquat (Eriobotrya japonica (Thunb.) Lindl.), ficus (Ficus microcarpa L. F.; Ficus benjamina L.), casuarina (Casuarina equisetifolia L.), weeping willow (Salix babylonica L.), flame coral tree (Erythrina coralloides DC.), privet (Ligustrum lucidum A. T. Aiton; Ligustrum japonicum Thunb.), cedar (Cupressus sempervirens L.), cypress (Cupressus lusitanica Mill.), Peruvian peppertree (Schinus molle L.), radiata pine (Pinus radiata D. Don), flagship pine (Pinus radiata var. binata (Engelm.) Lemmon), Mexican pinyon (Pinus cembroides Zucc.), palm (Phoenix canariensis Hort ex Chabaud.), yuca (Yucca guatemalensis Baker.) and rubber tree (Ficus elastica Roxb. ex Hornem.), trembling poplar (Populus tremuloides Michx.), swamp wattle (Acacia retinodes Schltdl.), wild black cherry (Prunus serotine Ehrn. ssp. Capuli (Cav.) Mc Vaugh), oak (Quercus acutifolia Née) and yucca (Yucca elephantipes Regel ex Trel.).

Field work

In order to know the general state of the study area, a preliminary tour was initially made in the Tezozomoc park with the help of a map provided by its administration. The different areas of the park were recognized, as well as their distribution and the type of aggregation of the trees; subsequently, a census of August 2009-2010 was carried out. From the botanical samples collected, the trees were identified based on the work of ^{Rodríguez and Cohen (2003)} and ^{Martínez and Tenorio (2008)}. Pine samples were taken to the Forest Entomology and Phytopathology Laboratory of Cenid Comef from the Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP).

Entomological material collection. The health status assessment considered 10 % of the most frequent species from the census carried out; of the less frequent species, all the individuals were included. Samples of leaves, branches, fruits and bark were taken; the technique of beating and direct collection was applied, as well as a tray with 70 % alcohol. The plant material was placed in plastic bags to prevent desiccation and insects collected in the field were stored in vial tubes with 70 % alcohol, immature forms, such as nymphs, larvae or pupae that were found at the time sampling was collected and kept in breeding chambers (boxes) with part of plant material in the case of nymphs and larvae, in order to obtain the adult phases; this procedure was carried out in the Pest Control Laboratory of the Facultad de Estudios Superiores Iztacala (Iztacala Graduate Studies School) where it was finally identified.

Laboratory work

Determination of pines. Cones, bark and needle samples were taken. Cross-sections were made of the latter and placed on slides to observe the arrangement and number of the channels in the optical microscope (Carl Zeiss Axiostar Plus) and contrast them with the keys of ^{Farjon et al. (1997)} and ^{Martínez (1948)}.

Entomological determination. The collected insects were observed under a stereoscopic Carl Zeiss Stemi 2000-C microscope and photographs were taken with a Canon Power Shot A640^® camera. The taxonomic determination was made at the family, genus and species level through the support of the taxonomic keys of ^{Ferris (1938)}, ^{Peterson (1973)}, ^{Stehr (1987)}, ^{Blackman and Easton (1994}, ²⁰⁰⁶), ^{Halbert (2001)} , ^{Triplehorn et al. (2005)}, ^{Bautista (2006)} and ^{Unruh and Gullan (2008)}.

The assemblies were made according to the characteristics and size of the organisms: the dry assembly was carried out using entomological pins (bed bugs and beetles), as well as by specialized techniques in slides with Canadian balm (aphids and scales). In the case of mites, direct assembly with Hoyer's liquid was used (^{Remaudière, 1992}; ^{Solís, 1993}; ^{Triplehorn et al., 2005}).

Statistical analysis

To process the data obtained from the mite and insect samples, the relative frequency (F) was used, which is considered as the number of times in which a species appears recorded at least once and is expressed as a percentage (^{Dix, 1961}), whose formula is:

Where:

mi= Number of sampes where one species appeared in the total number of samples (M).

To determine whether there is independence between the sanitary condition (insects and mites) and the physical state of the crown and the tree trunk, a χ² test was used with the following formula:

Where:

Σi=1…r (sum of the number of populations or rows of the contingency table)

Σj=1…c (sum of categories or columns of the contingency table)

Oij = Observed frequency per cell

Eij = Expected frequency per cell

The criteria used to determine the percentage of damage are based on the following categories: minimum (0 to 25 %), significant (26 to 50 %), Severe (51 to 75 %) and very severe (76 to 100 %) (^{Benavides, 1996}).

The hypotheses raised were the following:

Null hypothesis (Ho): the presence of insects or mites are independent of the physical condition of the trees.

Alternative hypothesis (Ha): the presence of insects or mites if it is dependent on the physical condition of the trees.

According to ^{Durán et al. (2005)}, the decision rule was applied to reject the null hypothesis (Ho): χ20> χ2α, (r-1) (c-1).

Tree composition

According to the census, in the Tezozómoc Park there are 3 758 trees made up of 30 species that are grouped into 16 botanical families, of which 15 are native and 15 exotic. Regarding the permanence of the foliage, it was observed that 67 % (20) are evergreen and 33 % (10) are deciduous (Table 1).

Determination of insects and mites

The phytophagous entomofauna and acarofauna grouped into 45 species included in 34 genera, 18 families and 6 orders (Table 2). The main eating habits of organisms are suckers (76 %) (Figure 2), which may be a consequence of the most abundant families being Aphididae (20 %), followed by Tetranychidae (13 %) (Figure 3); while, in the hosts the one that presented more phytophagous species was Salix bonplandiana (11), followed by Populus tremuloides (6) and Acacia retinodes (5) (Figure 4).

Figure 2 Percentage of damage caused by the phytophagus entomofauna (960 trees = 100 %). 

Figure 3 Species found on trees grouped by family. 

Sb = Salix bonplandiana; Sba = Salix babylonia; Sm = Schinus molle; Eg = Eucalyptus globulus; Ec = Eucalyptus camaldulensis; Ar = Acacia retinodes; Eco = Erythrina coralloides; Lj = Ligustrum japonicum; Fb = Ficus benjamina; Fu = Fraxinus uhdei; Pp = Pinus patula; Pa = Persea Americana; Qa = Quercus acutifolia; Cl = Cupressus lusitanica; Pc = Pinus cembroides; Pr = Pinus radiate; Prb = Pinus radiata var. binate; Pt = Populus tremuloides.

Figure 4 Percentage of hosts affected by insects and mites. 

The most frequent symptoms in the hosts were chlorosis or chlorotic points in the foliage, since the pathogens feed on the vascular tissue, mainly of the phloem, which causes the cells to collapse and block the passage of nutrients, in severe infestations cause premature fall of the foliage, in addition to the fact that most of these species produce honeydew (^{Cibrián et al., 1995}), (with the exception of mites) on which they develop fumagins, which are non-parasitic fungi, but live entirely of the honeydew produced by these insects, forming a dark and dense layer that reduces the amount of light that reaches the surface of the plant (^{Agrios, 2008}). This fumagina was most evident in Erythrina coralloides caused by Toumeyella erythrinae Kondo and Williams in all trees (100 %).

Despite the observed frequency of Aspidiotus sp. (83.67 %) in Acacia retinodes, the percentage of damage could not be determined, because this host showed other problems such as a micromycete and abiotic factors, so it could not be defined which factor is affecting its health condition. However, the damage caused by Icerya sp. was minimal (0-25 %), because it sucks the sap in the branches and its frequency was minimal (2.04 %) for this host.

Although Stenomacra marginella, Alebra sp. and Empoasca sp. were frequent, had no significant effects (0-25 %) on their hosts (Ligustrum japonicum (100 %), Ficus benjamina (23 %) and Populus tremuloides (45 %); the above can be explained as they are polyphagous, that is, they feed on different plant species: The opposite occurred in Salix bonplandiana in which the damage was severe (51-75 %) since it presented chlorotic points on the leaf caused by a set of Tetraniquid species: S. marginella (95 %), Alebra sp. (95 %), Empoasca sp. (95 %) and Corythucha salicata (20 %); the latter was also observed in Populus tremuloides (20 %), with minimal damage (0-25 %).

On the other hand, the incidence of diaspidids (possibly of the Chinaseis genus) in Pinus radiata (100 %), P. cembroides (29.6 %), P. radiata var. binata (41.3 %) was minimal (0-25 %), which may be related to the fact that low density was recorded in all these species. The presence of Tropidosteptes chapingoensis Carvalho (100 %) was significant (26-50 %) in adult trees, and severe damage (51 to 75 %) was observed in young trees with a leaf yellowing, and chlorotic stippling, - characteristic symptom of this species- and foliage shed by 50 %. However, these expressions may be associated with different biotic factors such as other phytophagous insects and even abiotic factors such as air or soil pollutants.

The damage caused by aphids was very low (0-25 %) in the hosts Cupressus lusitanica (1 %), Pinus radiata (1 %), Acacia retinodes (2.04 %), Populus tremuloides (3.8 %), Ficus benjamina (3.3 %). In Salix bonplandiana (25 % and 35 %) it was significant (26-50 %) because it presented three different species of the Aphididae family.

The effects associated with the Tetranychidae family in their hosts (Erythrina coralloides (20 %), Fraxinus uhdei (34.28 %) and Salix babylonica (26.3 %) were minimal (0-25 %), as were the damages caused by Blastopsylla occidentalis Taylor (34.45 %) found in Eucalyptus camaldulensis, since in both cases not many organisms were found per host.

About the mites and insects forming gills or cecidia, Aculops tetanothrix Nalepa, 1889 is consigned, which causes the leaves to form a hard red structure that surrounds the mites; gills cause the leaves to bend and be shorter than those not infested, which favors their premature fall (^{Cibrián et al., 1995}). This behavior is consistent with what was observed in the field in the Salix bonplandiana host in which the frequency was 100 %; in the same way, gills that were not red were recognized. The same symptoms produced by Aculops tetanothrix were identified in Schinus molle (100 %), but were caused by the psyllid Calophya rubra Blanchard, 1852 (100 %), with damage of 51 to 75 %, but without a severe infestation.

Organisms belonging to the Eulophidae or Aphelinidae family (65%) were found in some gills, since according to ^{Triplehorn et al. (2005)}, there is no great anatomical difference between these families, so it was difficult to define the family to which this wasp belongs; both have been reported as parasitoids, and there are no records on wasps of them mthat form gills in Salix bonplandiana. However, there are data on wasps belonging to the Eulophidae family, which are gill-forming in Ophelimus eucalypti Gahan, 1922 (species native to Australia) and in Chile in Eucalyptus spp. (^{Gómez et al., 2006}). The damage caused by these two phytophages in Salix bonplandiana was very severe (76-100 %). Another species belonging to this family is Quadrastichus erythrinae Kim, 2004, recorded in different species of Eritrina in Taiwan (^{Yang et al., 2004}).

Among the mites and insects that make gills, the aphid is characterized by forming them in the petiole; therefore, the passage of water and nutrients to the leaves is partially interrupted, which leads to yellowing and premature fall of the foliage. In Populus tremuloides the damage by this organism was minimal (0-25 %) since its frequency was low (1.51 %). But, because it is a deciduous species, it causes the early loss of foliage and the presence of gills in the leaves that have fallen.

The erryphid Acerya fraxinoflora (7.14 %) is a newly reported mite for Fraxinus uhdei (^{Otero et al., 1999}), which has caused significant damage (26-50 %) as it affects flower buds and manifests itself with deformation of the inflorescence in the form of gills and abortion of flowers. ^{García (1981)} described that the formation of these gills or cecidia resulted from the continuous stimulation of the invading organism, which uses the gill as a means to develop.

A genus of lepidoptera was also identified among defoliator insects: Lophocampa sp. on Schinus molle (2.41 %) and on Prunus serotina subsp. capulli. This lepidopter caused minimal damage (0-25 %) in its hosts, probably because they are more specific, since they are primary parasites that attack vigorous trees, and not individuals in a state of physiological deficiency (^{Dajoz, 2001}). This is not the main cause of defoliators having less frequency in the park, since they play an important role in food chains by transforming plant biomass into animal biomass and serving as food for numerous predators such as birds, which in the park are abundant (^{Martínez and Leyva, 2014}).

Another type of common damage is that caused by mining insects, which are characterized by forming a mine, path, channels or streamers in the leaflet since it feeds mainly on the leaf mesophyll and causes it to yellow (^{Méndez et al., 2008}).

Two miners were registered in the park, an undetermined diptera in Populus tremuloides (13.64 %) and a lepidoptera of the Gracillariidae family, possibly of the genus Phyllocnistis sp., in Salix bonplandiana (75 %). They were counted at the rate of three dipterans per leaflet, while the microlepidopteros only one per leaflet. The damage caused by these insects was 26 to 50 %. Collected dipterans were found dead inside the mine without traces of parasitoids, possibly due to the plant itself or to endophytic fungi (^{Cornell and Hawkins, 1995}), which can be explained because the defense chemicals are concentrated in the cuticle and in the cuticle. epidermis of the leaves.

In relation to the trunk, bark insects were less frequent, since they are only present when the trees are weakened by other factors, which, in extreme cases, results in the death of trees (^{Wood, 1982}). Two species belonging to the Curculionidae family were found, one (Dentrictonus adjuntus Blanford, 1897) on Pinus radiata var. binata (6.61 %) and Phloeosinus baumanni Hopkins, 1905 in Cupressus lusitanica (10.15 %); in both species they caused severe damage (51 to 75 %). These barkers are characterized by feeding on the tissues of the vascular cambium and the inner bark of the trees.

^{Cibrián et al. (1995)} indicates that Phloeosinus baumanni is not a primary pest for urban trees, but it becomes infested when it is weakened or in decline; they also mentioned that in Valle de México it is common to observe it on old trees of Cupressus benthamii and C lindleyi; however, these author do not specify location of plagued areas in the region nor percentage of damage.

NOM-019-SEMARNAT-2006 establishes that in Mexico there are bark insects of the Dendroctonus, Ips, Phloesinus and Scolytus genera, among others. Several of its species have an economic impact, to the extent that they are recognized as the most harmful forest pests in the country (^{Semarnat, 2012}). Of the genera mentioned in the norm, Phloesinus spp. was detected in this study. on the trees of Cupressus lusitanica.

Another type of damage that was infrequent and less representative in terms of the number of species corresponds to carpal ghosts of Specularius impressithorax (Pic), which affected only 5 % of the individuals of Erythrina coralloides. This bruquido feeds on the seeds of the color; its distribution in Mexico and the severity of its damage are unknown, since it is a poorly reported species (^{Romero et al., 2009}).

The value of α was 0.05; when the observed significance was greater, the null hypothesis (Ho) was accepted; in Acacia retinodes and Erythrina coralloides this hypothesis was accepted (Table 2), which means that the physical state of the crown is independent of the presence of insects and mites. In the case of the first species, other factors were observed that could influence their condition, such as exposed roots, because 16 % of the trees did not show foliage; while in E. coralloides the damage caused by the phytophagous did not influence the physical state of the leaves.

On the other hand, the physical condition of the crown of Cupressus lusitanica, Pinus cembroides, P. radiata var. binata, P. radiata, P. patula, Populus tremuloides, Salix babylonica, S. bonplandiana, Eucalyptus camaldulensis, E. globulus, Fraxinus uhdei, Prunus persica, Ligustrum japonicum, Schinus molle, Ficus benjamina and Yucca elephantipes was affected by the presence of those entomological agents.

In P. radiata var. binata, C. lusitanica, E. camaldulensis, S. molle, P. tremuloides, S. babylonica, S. bonplandiana, A. retinodes and E. coralloides, dependence was confirmed between the presence of bark beetles and the physical condition of the trunk.

The debarkers of P. radiata var. binata and C. lusitanica caused mechanical damage to the trunk; in S. molle, P. tremuloides, S. babylonica, S. bonplandiana, A. retinodes, E. coralloides and E. camaldulensis no debarking was found.