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Globally, coastal ecosystems are considered among the most vulnerable due to multiple factors associated with anthropogenic effects that have put the environmental services they provide at risk (Martínez & Psuty 2004, Miller et al. 2010, Duarte et al. 2013, Mendoza-González et al. 2016). Among these factors, urbanization associated with tourist activities is considered one of the most impacted because of the direct effects on the loss or fragmentation of original vegetation (Martínez & Psuty 2004, Grosholz 2002). However, in addition to these effects, the urbanization of coastal ecosystems has numerous indirect effects that increase their fragility. The arrival of invasive species is one of the most important indirect effects since it is one of the main causes of biodiversity loss and ecosystem degradation (Vilà et al. 2011, Simberloff et al. 2013, van Kleunen et al. 2018). It has been suggested that coastal ecosystems around the world are especially susceptible to the invasion of plant species (Castillo & Moreno-Casasola 1996, Grosholz 2002, Del Vecchio et al. 2015, Tordoni et al. 2021, Martínez et al. 2021). For example, in Mexico, it is estimated that nearly 9 % of coastal dune plant species are exotic (i.e., invasive or potentially invasive) (Martínez et al. 2021), although locally, this percentage could be higher (ca. 30 %; Parra-Tabla et al. 2018).
However, despite the growing evidence that shows the harmful effects of invasive species in coastal ecosystems (e.g., Hertling & Lubke 2000, Gallego-Fernández et al. 2019, Cai et al. 2020) and the increasing presence of these species, particularly in Mexican coasts, few studies focus on understanding the mechanisms that determine the invasion success (Ramírez-Albores et al. 2019, Martínez et al. 2021, but see Parra-Tabla et al. 2021). Coastal communities of the north of the Yucatan peninsula, characterized by their high species richness, phylogenetic diversity, and endemisms (Espejel 1987, Durán et al. 2007, Torres et al. 2010, Angulo et al. 2018), have been subjected during the last three decades to a severe deterioration that has promoted the arrival of an important number of exotic species (Parra-Tabla et al. 2018). Among these, the hemiparasite Cassytha filiformis L. (Lauraceae) stands out for colonizing a large part of the northern coast of the Peninsula and for attacking shrubs that are considered keystone species in Mexican coastal dunes, as well as in other coastal regions of the world (Nelson 2008, Ovando-Hidalgo et al. 2020, Cai et al. 2020, Hernández-Mendoza et al. 2023, Parra-Tabla et al. 2024).
In contrast with competitive interactions for resources that are established between native and invasive plants (Theoharides & Dukes 2007, Golivets & Wallin 2018, Traveset & Richardson 2020, Ni et al. 2021), invasive-native plants' parasitic interactions have been rarely studied (e.g., Cai et al. 2020). This kind of interaction is particular since the first barrier that an invasive parasitic species confronts when arriving in a new ecosystem is finding suitable hosts in which they can grow and reproduce. Although parasitic plants are typically considered generalist (Kelly et al. 1988, Press 1998, Callaway & Pennings 1998, Pennings & Callaway 2002), it has been reported that numerous parasitic plants show a certain level of specialization, or they switch during their life cycle to specialized use of host plants (Musselman & Press 1995, Kokubugata & Yokota 2012, Zhang et al. 2022). For example, parasitic species of the genus Cassytha (Lauraceae) occupy different hosts during their growth that only serve as a “bridge” until they find definitive hosts in which they sexually reproduce, thus ensuring the establishment and dispersion of their populations (Zhang et al. 2022).
Different characteristics such as the life form, the host plant architecture, and the parasite-host compatibility are determinants in the process of selection of an adequate host (e.g.,Press & Phoenix 2005, Kaiser et al. 2015, Li et al. 2015, Lara et al. 2021). Once parasitic plants are established, their hosts are expected to provide the parasites with the necessary resources to grow and reproduce. If this is the case, this selection should be reflected in the physiological performance of the parasitic plant. For example, an adequate host would be one that could offer sufficient resources such as water, and photosynthates (Kelly et al. 1988, Pennings & Callaway 1996, Koch et al. 2004, Lara et al. 2021). Thus, it could be predicted that a parasitic plant would prefer hosts that minimize water deficit and, in turn, can reduce its photosynthetic activity. Therefore, the success of an invasive parasitic plant will depend not only on host plant availability but also on the extent to which the hosts provide the necessary resources to establish long-term viable populations (Pennings & Callaway 1996, Press & Phoenix 2005).
On the other hand, the importance of the identity of the native host plant selected by the invasive parasites relies on the fact that it might be a crucial factor that determines the impact on the invaded ecosystem (Gibson & Watkinson 1989, Callaway & Pennings 1998, Cai et al. 2020. In this sense, if the invasive parasites attack hosts that play a key role in the community structure, their effect would be more critical than if they parasitize species that are not dominant or have a limited role in the community (Caviers 2021, Parra-Tabla et al. 2024). For example, some species are key in coastal communities as soil nutrient enrichers, nurse plants, or erosion controllers (Espejel 1987, Acosta et al. 2009, Hernández-Mendoza et al. 2023). In these ecosystems, it has been found that when invasive parasites attack these plants, their functionality is severely affected (Nelson 2008, Cai et al. 2020).
Although the pattern of spatial distribution of the invasive hemiparasitic species C. filiformis and its effects on some of the parasitized species are known on the northern coast of the Yucatan Peninsula (Parra-Tabla et al. 2024), the total range of hosts used by this species is unknown, as well as whether it shows any preference for the life form or species. It is also unclear whether there are differences in "host quality" regarding the physiological performance of C. filliformis when establishing and reproducing sexually. Filling these information gaps will help us to understand the mechanisms that allow invasive parasitic species to invade fragile ecosystems such as coastal communities.
In this work, we aim to answer the following questions: What is the host range used by the invasive parasite Cassytha filiformis in the coastal scrubland of northern Yucatan? Does C. filiformis show host preference? Does the physiological performance of C. fliformis (using water deficit and chlorophyll content as proxies) vary among hosts on which it establishes and reproduces?
Materials and methods
Study site and species. The study was carried out in an area of coastal scrubland located in Telchac Puerto, Yucatan, Mexico (21° 20′ 11.7″ N, 89° 20′ 12.5″ W; with an altitude from 0 to 8 m asl), during the months from October 2022 to June 2023. The coast's weather is hot semi-arid (BSh) with a mean annual temperature of 26 °C and an annual mean precipitation of ca. 350 mm (Orellana et al. 2009). The plan community is dominated by herbaceous species such as Agave angustifolia Haw. (Agavaceae), Alternanthera microcephala (Moq.) Schinz (Asteraceae), Waltheria rotundifolia Schrank (Malvaceae) and Melanthera nivea (L.) Small (Asteraceae) and shrub species such as Coccoloba uvifera L. (Polygonaceae), Scaevola plumieri (L.) Vahl (Goodeniaceae) and Suriana marítima L. (Suranaceae) (Espejel 1987, Angulo et al. 2018). In the coastal dune, nearly a third of all plant species are exotic (Parra-Tabla et al. 2018). Among these species, C. filiformis is the only parasitic species. Though it has been reported that C. filiformis is originally from Asia and currently has a pantropical distribution, botanical and phytogeographic studies from the decade of the 70’s or before do not register its presence in the Yucatan coastal ecosystems (Miranda 1959, 1964, Moreno-Casasola & Espejel 1986, Espejel 1987, Castillo & Moreno-Casasola 1996, Chiappy et al. 2001, GBIF 2022); therefore, it is considered an invasive species of recent arrival (Parra-Tabla et al. 2018, 2024).
Cassytha filiformis L. is an herbaceous hemiparasitic vine; filiform stems, measuring 0.4 to 3.0 mm in thickness, are either glabrous or bear trichomes, exhibiting a greenish or orange-yellow coloration. Leaves are alternate, reduced to sessile scales; the inflorescence takes the form of an axillary spike, comprising white or slightly greenish, hermaphroditic, trimerous flowers distributed along the inflorescence axis, the fruit is a whitish drupe (Silva et al 2021). It possesses haustoria, penetrating the host plants' stem tissue (Zhang et al. 2022) and absorbing nutrients, water, and photosynthetic products (Li & Yao 1992, Balasubramanian et al. 2014). It has been reported that C. filiformis occupies a wide range of hosts, with different life forms distributed in various environments such as grasslands, flooded forests, xerophilous scrublands, Mediterranean forests, and coniferous forests (Li & Yao 1992, Buriyo et al. 2015, Debabrata 2018, Zhang et al. 2022), as well as coastal dune vegetation, where it has been reported to prefer species of the genera Scaevola and Tournefortia (Nelson 2008, Castillo-Campos et al. 2019). In the Yucatan coastal dunes, it is known to preferentially attack species such as Scaevola plumieri (Goodeniaceae), Suriana maritima (Surianaceae), and Tournefortia gnaphalodes (Boraginaceae) (Parra-Tabla et al. 2024).
The damage C. filiformis causes to host plants is well documented, with effects ranging from reduced sexual reproduction to decreased survival (Zhang et al. 2022). Despite this, some physiological aspects of C. filiformis, such as its response to different hosts, have been largely overlooked. It is known that C. filiformis seedlings are autotrophic and can survive up to a month before parasitizing a viable host (Furuhashi et al. 2016). Like other parasitic vines, they grow in a creeping form, and upon encountering a potential host, they twine around the stem. If the host is viable, haustoria develops to penetrate the host tissue. Once established, C. filiformis can cover the host completely as it grows (Nelson 2008, Debabrata 2018). Even though it can establish on a host, C. filiformis may still move toward better-quality hosts, where it eventually reproduces sexually (Zhang et al. 2022). This hemiparasitic species does not produce leaves, and its stems slightly vary in color, displaying tonalities that range from yellowish or brown to light or dark greenish depending on the stem type (mature holding stems or young growing stems) (Figure 1). However, it is unknown whether variations in steam color are related to functional differences such as photosynthetic activity.
Figure 1 Young stems (A) and mature stems (B) of the hemiparasite Cassytha filiformis (Lauraceae) in the coastal scrubland in Telchac, Yucatan, Mexico.
Hosts identification of the hemiparasitic species Cassytha filiformis. A plot of 200 × 50 m (10,000 m2) parallel to the coast was established in a coastal scrubland adjacent to a coastal dune. In this plot, an inventory was made, and all plant species with a height above 30 cm were identified, recording whether they were parasitized or not by C. filiformis. The criterion to consider an individual parasitized was the presence of visible haustoria (Parra-Tabla et al. 2024). To determine persistent hosts and hosts in which C. filiformis produced flowers and fruits, this inventory was performed during the rainy season (October 2022) and during the dry season (May 2023), excluding species that presented only one parasitized individual. Based on these two inventories, the most frequently parasitized persistent species and those in which C. filiformis exhibited sexual reproduction were considered the "main" hosts. To confirm parasitism on the primary hosts and to describe haustoria development, histological analysis of transversal sections of host stems was performed in which C. filiformis haustorium presence was observed. Fresh samples was processed and embedded in paraffin blocks (Leica?). 5 µ sections of the paraffin-embedded samples were obtained with a semi-automated microtome (Thermo Scientific Microm HM310?) and mounted with resin for observation in a stereoscopic microscope coupled to a monitor (Olympus?).
Physiological parameters of Cassytha filiformis. Water potential.- To evaluate whether differences existed among C. filiformis relationships according to host species, water potential (ψ) was measured in young C. filiformis stems. As opposed to mature stems, young stems lack lateral growths, and their apical shape allows their handling for such measurement (Figure 1). In the three main host species recorded (see Results), three C. filiformis individuals growing on the host species were selected. For each C. filiformis individual, three ψ measurements (three stems per host plant) were performed using a Scholander bomb (SOLEN; model 1505D-EXP; USA). Samples consisted of 10 cm C. filiformis stem cuts.
Measurements were carried out pre-dawn (i.e., “ψpd”: ca. 5:00 a.m.), when there is a water balance between the plant and the atmosphere, and at afternoon n (i.e., “ψm”: ca. 13:00 p.m.) when there is higher water deficit (Knipfer et al. 2020). To consider initial ψ´s differences among host species, a rate of change between both periods of the day in which measurements were taken was performed applying the following formula: ∆ψ = (ψpd - ψm) / ψpd. The ψpd, representing the lowest water deficit, was considered the denominator to ensure that the values obtained for each host species were comparable.
Chlorophyll concentration.- To determine photosynthetic activity, the concentrations of chlorophyll a, b, and total chlorophyll produced in C. filiformis were measured in young and mature stems. Both stem types were randomly collected for three C. filiformis individuals for each main host species. The method described by Raya-Pérez et al. (2014) was used with some modifications. Four grams of plant tissue were measured and macerated in 10 ml of 80 % acetone. Subsequently, 5 ml of 80 % acetone was added, and samples were centrifuged at 3,500 rpm for 30 min (MicroCl 17R centrifuge). Finally, 8 ml of the supernatant was extracted and placed into quartz cells to be read in the spectrophotometer at 647 and 664 nm of visible light.
To calculate chlorophyll concentration, the formula by Leegood (1993) was used, with the chlorophyll extinction coefficients of Graan & Ort (1984) for 80 % acetone solutions: Chlorophyll a (µM) Ca = 13.19 × A664 - 2.57 × A647; Chlorophyll b (µM) Cb = 22.10 × A647 - 5.26 × A664; Total chlorophyll (µM) Ca + Cb = 7.93 × A664 + 19.53 × A. Finally, Arnon equations (1949) modified by Graan & Ort (1984) were used: Chlorophyll a mg/g of tissue Ca = (13.19 × A664 - 2.57 × A647) × V/1,000 × weight g; Chlorophyll b mg/g of tissue Cb = (22.10 × A647 - 5.26 × A664) × V/1,000 × weight g; Total chlorophyll mg/g of tissue Ca + Cb = (7.93 × A664) + 19.53 × A647) × V/1,000 × weight g; where A is the specific absorption coefficient at spectrophotometer wavelength in nm, V the volume in ml and the weight of the material used in grams. The mean of the samples was used to determine which host species influenced chlorophyll concentration the most, i.e., chlorophyll of young stems and mature stems.
The measurements of water potential and chlorophyll were performed at the beginning of the rainy season (June), which was the moment when C. filiformis produced flowers and fruits.
Data analysis. To test whether C. filiformis showed host preference according to their life form (herbaceous vs. shrub), a ψ2 test of independence (Zar 2010) was performed, which allows for weighting host abundances. After that, a ψ2 test of independence was carried out to test whether C. filiformis showed preference among the three main hosts.
To test differences in water potential at each time of the day and the ∆ψ among the host plant species, a generalized linear mixed model (GLMM) was applied, incorporating the time of the day, the host species, and the stem nested in each host as fixed factors. The stems were incorporated into the model to consider variation due to differences between stems. Each plant was considered a random factor. To test differences in chlorophyll a and b and the total chlorophyll among the host plant species and stem types (young vs. mature), a GLMM was applied with host species and type of stem nested in each host as fixed factors. In this analysis, each plant was also considered as a random factor.
All analyses were performed with the statistical package SAS v. 9.4 (SAS 2002). ψ2 tests of independence were carried out using the freq procedure (SAS 2002). GLMMs were evaluated using the glimix procedure (Littell et al. 2006). When differences were found among fixed factors, the functions pdiff and varcom were used (Littell et al. 2006) to estimate the percentage of variance explained by the nested level (host and stem type) for the chlorophyll concentration.
Results
Cassytha filiformis hosts. The results of the inventory in the rainy season showed that C. filiformis developed haustoria in 10 out of 18 plant species recorded. In the dry season, C. filiformis developed haustoria in 9 out of 14 species (Figure 2). The total number of parasitized individuals in the rainy season was 129, while 90 were in the dry season. The complete list of parasitized species is shown in the Table S1 and S2. The presence or absence of some species varied depending on the season. The species with the highest percentage of parasitism in both seasons were Scaevola plumieri (L.) Vahl (Goodenaceae), Pithecellobium keyense Britton (Fabaceae), Croton punctatus Jacq. (Euphorbiaceae) and Agave angustifolia Haw. (Agavaceae) (Figure 2). However, only in the first three shrubs it was observed that C. filiformis frequently exhibited sexual reproduction, and only one individual exhibited sexual reproduction in A. angustifolia; therefore, the three shrub species were considered the “main hosts”.
Figure 2 Percentage of individuals parasitized by Cassytha filiformis during the rainy season (A) and dry season (B) in a coastal scrubland community of Yucatan. The letter after the name of the parasitized species indicates the life form: herbaceous (H), and shrubs (S). Only species with more than 1 % of individuals parasitized are shown.
The ψ2 test showed that C. filiformis preferred shrub species (ψ2 1 = 24.0, P ψ 0.001). Less than 10 % of herbaceous species were parasitized and among shrub species, this percentage was above 30 % (Figure 3A). Among the main host, the ψ2 test showed significant differences in parasitism preference (ψ2 2 = 40.8, P ψ 0.001). The results suggested a preference by C. filiformis for P. keyense, in which nearly 90 % of all available individuals were parasitized (Figure 3B).
Figure 3 (A) Percentage of parasitized and non-parasitized individuals by life form for Cassytha filiformis in a coastal scrubland community of Yucatan. (B) Percentage of parasitized and non-parasitized individuals by C. filiformis of the main host species.
Histological analysis. The histological analysis corroborated the presence of haustoria penetrating the tissue of the main host species (C. puntatus, S. plumieri and P. keyense), showing observable differences in the morphology of each haustorium depending on the host (Figure 4). Although in all cases the haustoria appear to be in the cortex of the host, in the sample of C. punctatus (Figure 4D), a greater degree of penetration is observed, with haustoria closer to the vascular tissue of its host. In contrast, the samples of S. plumieri and P. keyense (Figure 4E and F) show more superficial penetration, with both C. punctatus and P. keyense exhibiting secondary growth in the host stem with S. plumieri specifically showing a thicker cortex layer.
Figure 4 Development ofCassytha filiformishaustoria on its main hosts in a coastal scrubland community of Yucatan. (A)Croton punctatus, (B)Scaevola plumieri, and (C)Pithecellobium keyense. The endophyte shows differences in terms of its shape, length, and depth of penetration (D, E, F). Tissue ofC. filiformis(asterisk), endophyte (green bracket), and host tissue (orange bracket) being observable. Additionally, the host epidermis is indicated (black arrow), withC. punctatus(D) andP. keyense(F) showing more secondary xylem growth (yellow arrow) than Scaevola plumieri(E) with more cortex and pith (red arrow).
Physiological parameters of Cassytha filiformis. Water potential did not significantly vary in any of the two time periods (pre-sunrise and afternoon) due to host identity (Figure 5A and B). However, statistically significant differences were observed in the ∆ψ (F 2,16 = 2.03, P = 0.03). The highest ∆ψ occurred in C. filiformis individuals growing on C. punctatus, and the lowest in individuals growing on S. plumieri (Figure 5C). The differences between these two hosts were significant (t = -2.87, P = 0.01). On the other hand, individuals growing on P. keyense did not show differences compared to C. punctatus or S. plumieri (t ≤ -1.5, P > 0.05).
Figure 5 Mean (± EE) of the water potential (A: predawn and B: midday) and change in water potential (ψ) (C) of Cassytha filiformis according to its host in a coastal scrubland community of Yucatan. Different letters indicate significant differences (P < 0.05) between hosts.
Differences were observed in total chlorophyll concentration (Table 1; Figure 6); the highest concentrations were found when C. filiformis was growing on C. punctatus or S. plumieri, which did not show significant differences between them (t 28 = 0.80, P = 0.42). The lowest chlorophyll concentration was found in P. keyense, which showed significant differences with C. punctatus and S. plumieri (t ≥ 2.6, P ≤ 0.01). Additionally, the analysis showed that chlorophyll a, b, and total concentration significantly varied according to stem age (young vs. mature) (Table 1). In all cases, the highest concentration was observed in young stems (Figure 7). The variance components analysis showed that the type of stem explained a higher percentage of the variance in total chlorophyll, as well as in chlorophyll a and b, concerning the percentage explained by the host identity (Table 1).
Table 1 Results of the nested GLMM model to test the effect of host species and stem type (young vs. mature) on the concentration of chlorophyll a, b, and total, of Cassytha filiformis in a coastal community of Yucatan. The percentage of variation explained for each case is shown.
| Chlorophyll | Factor | F | P | % |
|---|---|---|---|---|
| a | Host | 3.16 | 0.057 | 3.1 |
| Stem type (Host) | 25.9 | < 0.001 | 27.4 | |
| b | Host | 3.16 | 0.058 | 2.0 |
| Stem type (Host) | 16.3 | < 0.001 | 4.1 | |
| Total | Host | 6.61 | 0.004 | 12.3 |
| Stem type (Host) | 17.52 | < 0.001 | 36.4 |
Figure 6 Mean (± ES) of total chlorophyll concentration in both stem types of Cassytha filiformis according to the host they occupied in in a coastal scrubland community of Yucatan. Different letters indicate significant differences (P < 0.05) between hosts.
Figure 7 Mean (± EE) of a, b, and total chlorophyll concentrations between young and mature stems of Cassytha filiformis according to the host they occupied in in a coastal scrubland community of Yucatan. (A) Croton punctatus, (B) Pithecellobium keyense and (C) Scaevola plumieri. Different letters indicate significant differences (P < 0.05) between stem types in each host.
Discussion
The results of this work showed that the invasive hemiparasite Cassytha filiformis uses many host plants in the Yucatan coastal scrubland, preferring shrub species on which sexually reproduces. Furthermore, this work revealed differences in C. filiformis physiological performance across the main hosts. In general, the results suggest that C. filiformis’ host selection can be a relevant mechanism in the process of establishment of this species as it colonizes new environments.
Host range and preference of Cassytha filiformis. The results of this and previous work show that C. filiformis can parasitize up to 23 different species, including herbaceous and shrub species (Parra-Tabla et al. 2024). In particular, the results of the two inventories of this work added up to 8 host plant species, with the shrub species Pithecellobium keyense and Croton punctatus standing out for their high level of parasitism. Altogether, the results suggested that like several parasitic species (e.g.,Gibson & Watkinson 1992, Press 1998, Pennings & Callaway 2002), C. filiformis can be considered a generalist. However, the results also suggest that most species are used during short periods. In addition to preferring shrub species, C. filiformis selects a lower number of species on which it establishes and reproduces. In the genus Cassytha, the temporary use of hosts and the selection of definitive hosts seem common (Zhang et al. 2022). Specifically, for C. filiformis, it has been suggested that this species temporarily uses several host species as "bridges" that allow them to explore the environment until finding long-lifespan hosts (Zhang et al. 2022, Parra-Tabla et al. 2024). This has been explained because perennial species can provide long-term resources to parasitic species (Press & Phoenix 2005). However, even within a range of potential host perennial species, many parasitic species select a subset of these (Gibson & Watkinson 1989, Pennings & Callaway 1996). These observations suggest that despite the "generalist" status, several parasitic species have a certain level of specialization, behaving as discriminative consumers that increase the frequency of their parasitism toward “better hosts” (Kelly et al. 1988, Press & Phoenix 2005, Liu et al. 2023).
Specifically, in this work, we observe that C. filiformis preferred the shrub species P. keyense, C. punctatus and S. plumieri, regardless of the differences in abundance of these hosts. In these three species, C. filiformis showed sexual reproduction, and the histological study confirmed the development of parasitic structures. This evidence suggests that P. keyense, C. punctatus and S. plumieri are adequate long-term C. filiformis hosts. Therefore, in addition to the previous study that showed that in the coastal dune, C. filiformis prefers the shrubs Suriana maritima, Tournefortia gnaphalodes and S. plumieri (Parra-Tabla et al. 2024), this invasive parasite has at least five suitable shrub species available for establishment and dispersal, considering both the coastal dune and the scrubland. The relevance of C. filiformis parasitizing these shrubs is because these species are common or dominant in coastal dune and scrubland communities along the Yucatan Peninsula (Espejel 1987, Torres et al. 2010, Angulo et al. 2018). Furthermore, these species participate in soil fixation preventing erosion (Espejel 1987, Castillo & Moreno-Casasola 1996), and in the case of P. keyense, increase soil nitrogen concentration (Leirana-Alcocer & Bautista-Zuñiga 2014), besides playing the role of nurse plants (Ovando-Hidalgo et al. 2020, Hernández-Mendoza et al. 2023). Hence, it is possible that in the process of invasion in these coastal ecosystems, C. filiformis can provoke cascading effects that affect their functionality.
Different studies have documented that the damage caused by C. filiformis ranges from decreasing the sexual reproductive success of its hosts and increasing their mortality to inducing changes in the associations they establish with soil microorganisms (Nelson 2008, Prider et al. 2009, Cai et al. 2020, Zhang et al. 2022). In the coastal dune of Yucatan, parasitized S. plumieri, T. gnaphalodes and S. maritima individuals produce, on average, up to two times fewer flowers and fruits than non-parasitized individuals by C. filiformis (Parra-Tabla et al. 2024). This result suggests that C. filiformis has the potential to significantly decrease the reproductive success of the shrub species they parasitize, thus affecting the recruitment of new individuals via seeds. For this reason, future studies should consider the demographic impact on these species and the facilitation interactions (e.g., nursing) they promote to evaluate the effect of C. filiformis on the structure and functionality of the coastal plant communities of Yucatan.
Physiological performance of Cassytha filiformis. Hemiparasitic species such as C. filiformis depend highly on their host plants for water and nutrients to complete their life cycle. Therefore, these species must select hosts that give them adequate physiological performance. This performance is largely influenced by the microenvironment in which hosts are found. In semi-arid environments such as the coastal ecosystems of Yucatan, there is low water availability and variation among plant species in their ability to access this resource (Espejel 1987). In this sense, the host's identity can explain variables such as the water potential of parasitic plants, since in parasitic plants, stress for water deficit is experienced through the host (Zagorchev et al. 2021). No statistically significant differences were observed in C. filiformis pre-sunrise or noon water potential among the three main hosts in this work. This could indicate that the water status of C. filiformis is independent of the host. It is known that parasitic plants present high transpiration rates that cause stronger negative water potentials than the host, facilitating passive water transport (Ehleringer & Marshall 1995).
However, the analysis of the water potential change (∆ψ) showed significant differences among hosts, suggesting that the most drastic change throughout the day occurred when C. filiformis was established in C. punctatus and the lowest in S. plumieri. Considering that C. filiformis obtains its resources from the hosts, it is likely that the water redistribution of the soil-plant-atmosphere system that occurs naturally between night and pre-sunrise is modified to a soil-plant-parasite-atmosphere system. This result would explain the changes in water potential observed in C. filiformis throughout the day. In this context, in drastic temporary changes, water demand can lead to severe effects for both the parasite and the host (Watson et al. 2022). In this sense, the host in which haustoria penetrated the deepest was C. punctatus, and the most superficial was S. plumieri, which could be an indicator of the functional relationship between parasite and host.
In the relationship C. filiformis-C. punctatus, it is probable that, because of the ability of the parasite to penetrate the host, water exchange between them had been higher than with the other hosts. This can be confirmed by analyzing the water potential change (∆ψ), which was higher in C. filiformis-C. punctatus because as C. punctatus evaporative demand increases throughout the day, it could have affected the C. filiformis hydric status in two ways: by giving preference to the evaporative demand of the leaves or using part of C. filiformis water reserve to complement its water demand. In contrast, the relationship C. filiformis-S. plumieri, ∆ψ was lower, and this coincided with a lesser penetration of haustoria, suggesting that with deeper haustoria penetration, the relationship between the hydric status of the parasite and host strengthens. Although a follow-up of host plant survival was not carried out in this work, it was evident that C. punctatus individuals were the most affected (e.g., dead parasitized branches), which might be related to the degree of haustorium penetration into the host's tissue.
The results of this work also showed differences between hosts and stem types in total chlorophyll concentration, in addition to significant differences in the concentration of chlorophylls a and b in C. filiformis. Although the presence of chlorophyll in hemiparasites indicates some degree of photosynthetic activity (De la Harpe et al. 1981), chlorophyll concentration does not necessarily indicate higher or lower photosynthetic activity (Amutenya et al. 2023). However, previous studies reported that this is considered functional despite low chlorophyll concentration in C. filiformis (De la Harpe et al. 1981, Balasubramanian et al. 2014). Chlorophyll in hemiparasitic plants allows them to have a nutrient source while searching for hosts or starting to grow on them (Press et al. 1988, Zhang et al. 2022). At the same time, it permits them to adjust to hosts that show variations in the amount of nutrients they can provide. In C. filiformis, the highest chlorophyll concentration was observed on C. punctatus and the lowest on P. keyense, suggesting that C. filiformis has a higher photosynthetic activity on C. punctatus. This result is additionally supported by the low concentration of chlorophyll b observed, compared to chlorophyll a, since the latter is the primary photosynthetic pigment. In contrast, type b is an accessory pigment that participates in light absorption at shorter wavelengths (Masuda & Fujita 2008).
In other hemiparasitic species such as Thesium chinense (Santalaceae) and Rhinanthus alectorolophus (Orobanchaceae), it has also been observed that chlorophyll concentration depends on host plant identity (Luo & Guo 2010, Moncalvillo & Matthies 2023). Differences in the concentration of the chlorophyll produced by hemiparasitic plants in different hosts reflect the complexity of their nutrition process. For example, in several species of mistletoe, resources obtained through the xylem of the host are mostly inorganic solutes and water, while nutritional elements such as carbon or elements for lipid synthesis are produced by the hemiparasite via photosynthesis (Ehleringer et al. 1985, Švubová et al. 2013). In this sense, the photosynthetic activity of these species might be a path of compensating for resources it does not obtain from the host. For example, carbon assimilation occurs through the host and the parasite in the species Cassytha pubescens (De la Harpe et al. 1981, Prider et al. 2009, Těšitel 2016).
In C. filiformis, it has been reported that haustoria can access not only the xylem but also the phloem (Balasubramanian et al. 2014, Zhang et al. 2022), which in principle allows C. filiformis to take carbon directly from its hosts. Thus, C. filiformis would not need to perform photosynthetic activity to fix carbon, thus low chlorophyll concentrations would be expected. Nevertheless, the differences observed among hosts suggest differences in C. filiformis photosynthetic activity among hosts and differences in host "quality" based on the amount of photosynthates the parasite can obtain. Future studies that associate these differences with the growth, survival and reproductive success of C. filiformis will allow us to elucidate the ultimate consequences of host selection by this species.
On the other hand, a noteworthy result of this study was that differences were observed in chlorophyll a, b, and total concentration between young and mature C. filiformis stems. To our knowledge, this has not been reported before in other parasitic species. These differences suggest functional differences where mature stems that serve as support could be taking more resources from the host. In contrast, exploring and growing on the host, young stems would probably need to complete their requirements through a higher photosynthetic activity. This interpretation is consistent with evidence that suggests that in the first stages of its life cycle, C. filiformis might have sufficient photosynthetic activity while exploring and finding viable hosts through its growing stems (Furuhashi et al. 2016). However, the differences in concentrations and proportions of a and b chlorophylls might result from other factors and cannot be dismissed. For example, it is known that chlorophyll b concentration is related to plant photo-protective mechanisms (Voitsekhovskaja & Tyutereva 2015), which in environments exposed to high radiation, such as tropical coastal environments, could be playing an important role.
We acknowledge the limitations of our results, as we only evaluated the water deficit and chlorophyll content of C. filiformis on different hosts. However, as an initial approach to studying its physiological performance on different hosts, we can say that the overall results of this work regarding C. filiformis' preference and physiological performance highlight the need for future studies to analyze in detail aspects such as host-parasite water and nutrient flow, and the specific nutrients transferred from host plants to C. filiformis. These studies would elucidate the importance of nutritional factors in host selection by C. filiformis, helping to explain its success as an invasive species in coastal ecosystems.
In conclusion, this work shows that the coastal invasive hemiparasitic species C. filiformis has many available host species, among which selects those whose physiological and reproductive performance is most suitable, probably increasing its invasion success.
Supplementary material
Supplemental data for this article can be accessed here: https://doi.org/10.17129/botsci.3529.
