Nuisance Growth of Cissus verticillata (Vitaceae) Negatively Affects the Structure of Mangroves in Marismas Nacionales Nayarit, Mexico

Abstract

Changes in the structure and composition of mangroves may be influenced by anthropogenic and natural causes. Mangrove coverage in Marismas Nacionales Nayarit –a Biosphere Reserve in northwestern Mexico—has declined in the last decades, mostly related to human activities (e.g., opening of the Cuautla inlet) and climate variability (e.g., El Niño Southern Oscillation and hurricanes), leading to diverse ecological and socioeconomic consequences. This contribution reports the impact of Cissus verticillata—a climbing plant species—in the structure of mangroves distributed in this Natural Protected Area during 2019 and 2022. Forest structure analysis was compared in four plots of 20 m × 20 m each, all of them influenced by San Pedro Mezquital river. Two plots (Unión de Corrientes) showed the presence of Cissus verticillata, while two nearby plots (Boca de Camichín) recorded no presence of this species. A poor mangrove structure, no natural seedling recruitment and high mortality was observed in those sites with the presence of C. verticillata. These results highlight the vulnerability of mangroves to C. verticillata in Marismas Nacionales Nayarit Biosphere Reserve, which in addition to other human and climate stressors may compromise its ecological integrity in the future.

1. Introduction

Mangrove forests are considered one of the most important wetlands for the multiple ecosystem services they provide, e.g., natural barriers, biological filters, and high productivity refuge for species of commercial importance in some parts of their life cycle. Their physiological adaptations (e.g., aerial roots, salt-secreting glands, and viviparity) make them highly resilient species to changing environments [1]. Mangrove coverage in Mexico is ranked fourth globally [2]. According to official cartography, mangrove coverage has shown a recovery in 2015–2020; however, some states in northwestern Mexico showed an opposite trend, e.g., Nayarit reported a loss of 247 ha for the same period and was third in greatest loss after Sinaloa and Baja California Sur [2].

Marismas Nacionales is a Natural Protected Area under the category of Biosphere Reserve, and the Ramsar site located in Nayarit, Mexico (Figure 1). It is considered one of the most important wetlands in the country due to its ecological complexity. Historical changes in this lagoon complex have been mostly associated with human activities (e.g., opening of the Cuautla inlet), climate and weather events (e.g., Rosa hurricane, 1994; Roslyn, 2022), causing soil erosion or sedimentation, and changes in salinity levels.

Although the vulnerability of mangroves is mainly associated with anthropogenic activities like logging, contamination from wastewater discharges, industrial and urban development, livestock, agriculture, etc., there are other factors that may cause damage, even irreversibly, affecting the structure of these forests, such as pests, where most of the studies have been related to investigating the impacts caused by fungi [3], herbivory [4], and the introduction of invasive plants [5] or even nuisance species, i.e., native species with rapid growth that may cause negative environmental or economic impacts.

The decrease in salinity in some areas in Marismas Nacionales has been associated with changes in the hydrological system [6] that may create favorable conditions for the establishment of some species to new areas. This could be the case for Cissus verticillata, commonly known as possum grape vine and locally as “tripa de zopilote”. C. verticillata is a perennial native species from Mexico, Central America and the Caribbean, whose distribution in this country is considered cosmopolitan, and although it is part of the natural flora of deciduous forest ecosystems, its presence in mangroves has a nuisance growth [6,7,8]. Invasive species or invasive alien species are terms frequently used in the literature to report nonnative species that cause various negative impacts (ecological, economic, or related to human health), e.g., [5]. However, C. verticillata is native to the study area, therefore nuisance species is suggested as a more appropriate term.

C. verticillata is a climbing species, with medicinal uses, is deciduous and easy to propagate, and it has easily adapted to tropical climates; its seed size reaches a maximum of 1 cm, and they survive in the intestine of the birds after being consumed [6,8,9,10]. Propagation routes are very easy through cuttings, seed transport through streams, and birds [8,11]. Recently, the presence and cover change of C. verticillata was evaluated in Marismas Nacionales Nayarit using satellite-derived multispectral data, reporting an increase of 426.2 (2019) to 838.1 ha (2021), mainly identifying its presence in nearby areas to Acaponeta and San Pedro Mezquital rivers [12].

Mangrove structure is determined by the dispersal of propagules, species composition, zonation, growth and survival, although there are other factors that may change its structural composition, e.g., damage caused by storms, tidal influence, sedimentation, nutrients, and microtopography [13,14]. The evaluation of the different structural attributes contributes to the identification of the level of development and vulnerability of mangrove ecosystems. The hypothesis of this study is that the presence of C. verticillata induces poor structural development of mangroves in the affected areas within the Biosphere Reserve. The aim of this research was to investigate the impact of C. verticillata by comparing structural attributes, mortality and natural regeneration between sites with and without the presence of this species.

2. Materials and Methods

2.1. Study Area

Marismas Nacionales Nayarit Biosphere Reserve (hereafter referred to as MNNBR) (it was decreed in 2010; Figure 1) is integrated by a complex of diverse ecosystems, such as coastal lagoons, swamps, marshes, and mangrove forests. Each of these areas are important due to their specific conditions such as the hydrodynamics, influence of rivers, artisanal fisheries, and communities settled in surrounding areas. Mangrove coverage (Figure 1, panel 3) corresponds to 15–20% of the national total, which is equivalent to ~113,000 ha [15].

MNNBR is characterized by a semi-warm and sub-humid climate with an average annual temperature of 26 to 28 °C, an average maximum temperature of 30 to 34 °C and an annual precipitation of 800 to 1200 mm. The hydrographic system of MNNBR is complex, e.g., it is influenced by rivers, groundwater and ocean waters through tidal influence. The conditions of this lagoon complex, such as silty soils, brackish water, and high average temperatures, are optimal for the establishment of mangrove communities of the four characteristic mangrove species found in Mexico, i.e., Rhizophora mangle (red mangrove), Laguncularia racemosa (white mangrove), Avicennia germinans (black mangrove), and Conocarpus erectus (buttonwood mangrove). The zonation is represented by red mangrove at the edge of the channels, followed by white mangrove and black mangrove, while patches of buttonwood mangrove are found in areas where salinity is lower [16]. Nevertheless, local environmental conditions may modify this distribution.

This research is part of the Mexican Mangrove Monitoring System led by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), to investigate structural attributes and ecological indicators for 12 plots (20 m × 20 m) located within the reserve. This contribution focused solely on comparing (March 2019 and November 2022) structural attributes, natural regeneration and mortality of mangroves, considering sites with no presence of C. verticillata (Boca de Camichín) and another one notably affected by this species (Unión de Corrientes) (two plots each; a detailed description is shown in the next section). The sites were all located in the tidal basin of Boca de Camichín-Mexcaltitán, in the southern region of MNNBR (Figure 1, panels 2 and 3). Central coordinates, local names and sampling dates for this study are specified (

Table 1. Central coordinates and sampling dates corresponding to the study sites.

Plot	Local Name of the Site	Latitude	Longitude	Sampling Dates
A	Boca de Camichín	21.832292	−105.477975	25 March 2019; 14 November 2022
B		21.768176	−105.50823	26 March 2019; 14 November 2022
C	Unión de Corrientes	21.972358	−105.510564	27 March 2019; 18 November 2022
D		21.983529	−105.474844	28 March 2019; 18 November 2022

).

2.2. Forest Structure

For this study, four sites along MNNBR were chosen to compare the impact of C. verticillata in the structure of mangroves. At each site a 20 m × 20 m plot was delimited, named A, B, C and D (Figure 1-panel 3), two of them without the presence of C. verticillata (A and B plots in Boca de Caimichín) and the other two plots with the presence of this species (C and D plots in Unión de Corrientes). The analysis of forest structure was carried out following the method developed by Valdez-Hernández [17]. Only stems with a diameter at breast height equal to or greater than 2.5 cm were considered, recording the following structural attributes:

Mean height (m): It is a variable that defines the development of mangrove forests and was measured with a Nikon Forestry 500 hypsometer.

DBH (Diameter at Breast Height) (cm): This is a standard measure at a height of 130 cm (here and after referred to as DBH) using a diameter tape [18]. DBH is a common metric for monitoring forest structure in ecological studies. In the case of Rhizophora mangle, DBH was measured above the highest stilt root.

Density (stems ha⁻¹): Indicates the number of stems per unit of area.

Basal Area (BA) (m² ha⁻¹): It is a parameter that indicates the available volume of wood and is determined using the equation: BA = π/4((DBH/100)²) × 10,000 [19,20].

Importance Value Index (IVI): This attribute is used to determine the importance of the species in each sampling area and is calculated with the following formula [21]:

IVI = Relative density + Relative dominance + Relative frequency

where

$$\mathrm{Relative} \mathrm{density}={\displaystyle \frac{density of a species}{total density of all species}}\times 100$$

$$\mathrm{Relative} \mathrm{dominance}={\displaystyle \frac{Total basal area of a species}{Total basal area of all species}}\times 100$$

$$\mathrm{Relative} \mathrm{frequency}={\displaystyle \frac{Number of ocurrences of a species}{Total number of ocurrences of all species}}\times 100$$

Holdridge Complexity Index (HCI): This index is used to determine the degree of structural development of mangrove forests and was calculated with the equation HCI = h × ba × d × ns/1000, where h = height (m); ba = basal area (m² 0.1 ha⁻¹); d = density (stems 0.1 ha⁻¹); and ns = number of species [22].

2.3. Statistical Analysis

Differences between the means of the structural parameters (DBH and height) were tested using a one-way ANOVA analysis. A post hoc analysis was then performed using a Tukey HSD test to determine differences between groups of plots. Statistica software v. 8.0 was used for data processing [23].

2.4. Natural Regeneration and Mortality

Natural regeneration was evaluated for each plot (four 1 m × 1 m quadrants each) and all individuals with a height ≤ 1.3 m were considered as seedlings. In relation to mortality, density, mangrove species and cause were recorded, i.e., natural (here natural mortality was referred to average interaction between mangroves and their environment; see [24]) or logging.

3. Results

3.1. Density of Mangrove Species

This attribute varied between plots during 2019 and 2022. Density was higher during both stages in A and B plots (Boca de Camichín) with 2075 and 2050 stems ha⁻¹ respectively during 2019 showing a lower density during 2022, i.e., 1875 and 1690 stems ha⁻¹, respectively. On the other hand, C and D plots (sites characterized by a higher influx of the San Pedro Mezquital river)—showed a lower density, with 660 and 850 stems ha⁻¹, respectively during 2019, while a mangrove density of 530 was observed for C plot during 2022 (

Table 2. Density (stems ha⁻¹) and relative density for four plots during two sampling stages (2019, 2022).

Plot	Density (Stems ha−1)		Relative density (%)
			Lr	Ag	Rm	Lr	Ag	Rm	NI
	2019	2022	2019			2022
A	2075	1875	49	33	18	58	27	15	1
B	2050	1690	46	48	6	37	54	9	0
C	660	530	42	58	0	47	53	0	9
D	850	Unrecorded	65	35	0	Unrecorded

Lr: Laguncularia racemosa; Ag: Avicennia germinans; Rm: Rhizophora mangle; NI: not identified.

). It is emphasized that D plot was highly affected by C. verticillata covering the mangrove canopy almost in its entirety during 2022, and therefore stems were not able to be counted or measured (see Figures S1 and S2; Supplementary Materials). As discussed later, a 100% mortality may occur under such conditions.

3.2. Height and DBH

Mean height showed significant differences between plots in both stages (p < 0.05). A plot showed the highest mean height in 2019 (9.1 ± 0.32 m) (Figure 2a), while the lowest average was observed for C plot (2.2 ± 0.21 m) in 2022 (Figure 2b). For DBH, the highest mean was recorded for A plot (10.3 ± 0.71 cm) in 2022 (Figure 3a), while the lowest average was observed for D plot (3 ± 0.14 cm) in 2019. Differences for DBH were significant between plots (p < 0.05) in both stages (Figure 3a,b).

3.3. Basal Area, Holdridge Complexity Index (HCI) and Importance Value Index (IVI)

The highest basal area was observed in A plot during both stages (2.01 and 2.08 m² 0.1 ha⁻¹ for 2019 and 2022, respectively), followed by B plot (1.83 m² 0.1 ha⁻¹ in 2019 and 1.80 m² 0.1 ha⁻¹ in 2022), while C and D plots recorded the lowest values. The species with the highest value of this forest attribute was A. germinans for B plot (1.3 m² 0.1 ha⁻¹ in 2019 and 2022), while the lowest records corresponded to R. mangle in B plot (0.02 m² 0.1 ha⁻¹) during 2019. The highest IVI values were observed for A. germinans (C plot during both years). In relation to HCI, these values coincide with the structural characteristics of each plot, i.e., the highest HCI were recorded for A and B plots during both sampling years with no presence of C. verticillata, while C and D plots showed the lowest HCI, low density, and were widely covered by this climbing plant. Individuals whose species was not identified due to severe damage were not included in the analyses (

Table 3. Basal area, IVI and HCI of mangroves of four plots located in Marismas Nacionales Biosphere Reserve Nayarit during 2019 and 2022. BA = Basal area; IVI = Importance Value Index; HCI = Holdridge Complexity Index. HCI, density and basal area were calculated for 0.1 ha. * No individuals were measured within the plot in 2022 due to the wide coverage by Cissus verticillata.

Plot	Species	BA m2 0.1 ha−1		IVI		BA by Plot m2 0.1 ha−1		HCI
		2019	2022	2019	2022	2019	2022	2019	2022
A	Laguncularia racemosa	0.84	1.07	140	167.5
	Avicennia germinans	1.07	0.93	118	98.4	2.02	2.09	11.39	6.48
	Rhizophora mangle	0.11	0.09	42	34.1
B	Laguncularia racemosa	0.47	0.43	120	98.1	1.83	1.80	7.16	5.3
	Avicennia germinans	1.34	1.32	167	183
	Rhizophora mangle	0.02	0.03	13	18.9
C	Laguncularia racemosa	0.05	0.03	117	128	0.16	0.09	0.08	0.02
	Avicennia germinans	0.11	0.06	183	172
D	Laguncularia racemosa	0.04	*	181	*	0.07	*	0.04	*
	Avicennia germinans	0.03		119

).

3.4. Mortality and Number of Seedlings

The highest density of dead individuals was observed during 2019 for C plot with 1125 stems ha⁻¹. Trees in this plot were widely covered by C. verticillata during that year with a notable extent during 2022 (see Figure S2, Supplementary Materials), and L. racemosa was mainly affected. D plot recorded a mortality of 300 stems ha⁻¹ during 2019, also associated with C. verticillata. D plot was widely covered by C. verticillata during 2022, and therefore stems were unavailable to be measured, and mortality was underestimated (Figure 4; Figure S2, Supplementary Materials).

Mortality was predominantly associated with natural causes for all sites and stages, with the highest record in C plot during 2019 (1125 stems ha⁻¹). The site with the lowest mortality was B plot, recording 100 dead stems ha⁻¹ for both stages, 50% related to logging in 2019 and decreasing to 25% during 2022 (Figure 5). Natural mortality for A and B plots might be associated for 2022 due to the impact of hurricane Roslyn, which made landfall in MNNBR on 23 October 2022 as a category 3.

Again, it must be noted that many stems were not counted due to the high coverage of C. verticillata in C and D plots (see Figure S2, Supplementary Materials).

The most vulnerable species was L. racemosa, particularly in A (2022), C (2019), and D plots (2022) (Figure 6); however, it must be emphasized that many dead individuals could not be identified by species due to high damage (NI) in the case of A and B plots, or high coverage by C. verticillata as occurred in C and D plots (Figure S2, Supplementary Materials). Stem damage in A and B plots could be associated with the impact of hurricanes Willa (October 2018) and Roslyn (October 2022).

Natural regeneration was observed only for A and B plots in 2019 (an average of 8750 and 4375 seedlings ha⁻¹, respectively) while no seedlings were observed in any of the sampling plots during 2022.

4. Discussion

The presence of C. verticillata within MNNBR and its impact on mangroves is an important theme to be considered in the conservation agenda. C. verticillata is a tropical species with discussed medicinal effects and has been used as a natural remedy for diabetes and respiratory problems, as well as having others benefits [25,26]. Its distribution in Mexico is wide [7] and it has been found in mangrove ecosystems without representing any risk [27]; however, as shown in this study, its presence in mangroves distributed in some areas in MNNBR is considered aggressive.

The structure of mangroves was analyzed for eight additional plots distributed along this Natural Protected Area n and the presence of C. verticillata was observed in C and D plots only (this study), located in the Union de Corrientes area. The study sites in this contribution are influenced by the San Pedro Mezquital river, i.e., their main freshwater tributary and probably the main route of introduction for C. verticillata seeds. In addition, this species easily reproduces through cuttings. Another vector for the propagation of the seeds could be related to birds that inhabit this wetland complex [8]. Also, it is important to mention that mangrove communities settled in the lagoon and waterways are influenced by agricultural activities, so runoffs loaded with fertilizers and discarded from those areas can be another factor that promotes the growth and spread of C. verticillata.

According to Valderrama-Landeros et al. [12], C. verticillata was first detected in the mangroves of Marismas Nacionales Nayarit in 2017; however, anecdotal evidence suggests its presence for the past 40 years [6]. This species has been reported at different points throughout MNNBR, in which both its wide spread and freshwater runoff as its main route of introduction were noted [6,12,28]. The sites reported in these studies (located in the Mexcaltitán area) receive runoff from nearby rivers, mainly a current of the San Pedro Mezquital river which has influence into the plots where C. verticillata was observed in this study, or are located close to crop areas, which favors the development of C. verticillata. Its presence is therefore related to areas with a direct influx of freshwater [6].

Within this same lagoon complex, researchers have reported the presence of invasive plants like Arundo donax and Cenchrus ciliaris [6], mainly affecting the cycle of nutrients and hydrology of the wetlands, as well as displacing native species. This is considered a serious problem since they spread easily through different vectors such as runoff, wind, birds, and in the case of A. donax, by rhizome division; however, there are no records of their direct invasion of mangroves as observed in C. verticillata.

This climbing species causes changes in mangrove structure, since it usually covers crown and stems almost entirely, preventing the entry of sunlight and therefore affecting photosynthesis, growth and survival, and at the same time increasing mortality levels and preventing the establishment of seedlings. Also, C. verticillata competes with mangroves for nutrients from water, limiting growth and proper development until individuals die of suffocation [6,12].

According to our results, height and DBH values were higher for A and B plots compared to C and D parcels, which as discussed are in areas covered by C. verticillata. The second-highest mean height value was 6.6 m (B plot), a similar value reported by [29] in Huizache-Caimanero, Sinaloa, i.e., a height of 6.4 m and DBH of 12.4 cm, which was higher in comparison to the highest value recorded in this study (10.2 cm in 2022), which might be explained by the structural maturity of the Huizache-Caimanero system. According to [30] the relationship between density and DBH is expected to be inverse; however, in this study both attributes were low in the sites with a presence of C. verticillata, which is another piece of evidence of the structural changes associated with this climbing species and derived mortality. In addition, hurricane Roslyn made landfall in MNNBR on 23 October 2022 which also affected the structure and survival of mangroves in the study area.

The highest density was observed in A and B plots (2075 and 2050 stems ha⁻¹ respectively during 2019), and the most abundant species was L. racemosa. These results are comparable with those reported by [31] in La Encrucijada, Chiapas, i.e., 2103 stems ha⁻¹ for the same species plus R. mangle and A. germinans. These results corresponded to a dense and healthy forest, which is not observed in C and D plots, where mangroves were widely affected by C. verticillata. On the other hand, this species has also been reported to affect Rhizophora mangle along the banks of the San Pedro Mezquital River [12].

Basal area was higher in A plot in 2022 (2.09 m² 0.1 ha⁻¹), associated with its higher structural values of DBH and density. The lowest values present in C and D plots (<0.17 m² 0.1 ha⁻¹) were lower than those reported by [32] in Huizache-Caimanero, Sinaloa, which observed a basal area of 1.4 m² 0.1 ha⁻¹.

The highest values of the IVI were observed for A. germinans (C plot) and L. racemosa (D plot) with 173 and 167, respectively. These results were higher than reported by [33] for A. germinans in Laguna Mecoacán, Golfo de Mexico, with an average value of 63.

The HCI is used to integrate structural attributes, e.g., when the value is lower, the complexity decreases and therefore the mangroves are more vulnerable. A plot recorded the highest value, comparable with Teacapán, Sinaloa (HCI = 10.6), reported by [34], which corresponded to a site with similar characteristics (mixed and riverine forest). A and B plots recorded the three most abundant and common mangrove species on the Mexican Pacific coast, while C and D plots did not record red mangrove R. mangle—although it has a presence and is also affected by C. verticillata in nearby sites, as mentioned earlier [12]. These last two plots have low structural development, explained by their low HCI and BA values.

Mortality was one of the most important indicators to evaluate the damage caused by C. verticillata on mangroves in MNNBR. The high mortality observed in C and D plots is an example of the impact of this climbing species on those species. Mortality due to natural causes is diverse in the case of mangroves, either due to physical–chemical changes, natural events like hurricanes, erosion processes, among others; and according to our results, the likely source of mortality in such parcels was mostly related to the presence of C. verticillata. As mentioned earlier, C. verticillata competes with the mangroves for nutrients and light while covering its crown, and eventually most of the mangroves die. Although the species of several mangrove trees could not be identified due to damage, it was observed that the white mangrove L. racemosa was the one that presented the highest mortality, which coincides with other authors [6,28].

Another health indicator of an ecosystem is natural regeneration. C and D plots showed no establishment or growth of mangrove seedlings in any sampling. The explaining factors can be diverse, such as changes in the hydroperiod, anthropogenic activities that prevent natural regeneration, contamination, variations in the physical–chemical parameters, among others; however, in this study, C. verticillata may explain this result.

Another indirect effect caused by this species is its socioeconomic impact. As widely discussed, mangroves are nursery areas for many species with commercial importance (e.g., shrimp, fish), and therefore the presence of C. verticillata could affect the derived ecosystem services for many rural communities when mortality occurs. In addition, it has been found that this species is host to Maconellicoccus hirsutus (Green, 1908), a plague that attacks plants such as beans and corn, fruit trees, ornamental plants—among others—becoming a threat to agriculture [28], which is one of the main activities that take place in northwestern Mexico.

It is important to mention methods that have been used to control C. verticillata in the MNNBR. A program was developed for early detection and rapid response, in which different strategies were proposed for its reduction, integrating the participation of associations, government agencies, and residents of the communities surrounding the region [6], but there are no records of a follow-up to this program. As a control measure, in cases where C. verticillata has affected fruit and vegetable crops, the use of herbicides such as glyphosate has been proposed; however, it showed tolerance and a difficulty being controlled [35]. The removal method has been manual and performed by local people in MNNBR, [6], but this has not been efficient either. In the present research, C. verticillata widely covered C and D plots during 2019 and 2022 (Figures S1 and S2; Supplementary Materials). New control strategies are necessary, as the presence of C. verticillata may affect additional areas in MNNBR, in addition to the loss of mangrove coverage and ecosystem services for local communities.

5. Conclusions

Although C. verticillata is a native species, it has been reported to have wide growth on mangroves. Based on this, the hypothesis proposed in this study was tested, demonstrating the poor structural attributes and high mortality of mangroves located in sites with the presence of C. verticillata in MNNBR for both sampling years (2019 and 2022).

A and B plots (showing no presence of C. verticillata) recorded a higher structural complexity as shown in the attributes height, DBH, density, density of seedlings, and Holdridge Complexity Index. In contrast, C and D plots were covered by this climbing species, which had direct effects on the development of mangroves by blocking sunlight and affecting their development, causing them to show poor structural attributes, high mortality and no natural seedling recruitment. The main causes of its spread could be related to the higher influence of freshwater runoff from the San Pedro Mezquital river, and vectors such as birds. A frequent method of control and management for C. verticillata has been manual removal, though this approach has not proven efficient either; therefore, novel control strategies for C. verticillata must be implemented to prevent a wider spread within this Biosphere Reserve and avoid further significant loss of mangrove coverage.