Are southern pine forests becoming too warm for the southern pine beetle?
Graphical abstract
Introduction
The southern pine beetle (Dendroctonus frontalis Zimmermann; Coleoptera: Curculionidae) is one of the most aggressive tree-killing insects in the world (Vega and Hofstetter, 2015). Within its historic distribution in the southeastern United States, losses to the forest products industry exceeded $1 billion for 28 years ending in 2004 (Pye et al., 2011) and this, along with the loss of property value and recreation space, are only some of the effects of D. frontalis on forests and people (Coulson and Klepzig, 2011; Coulson and Meeker, 2011).
In most years, in most forests, D. frontalis is a rare and relatively benign component of the forest insect fauna that primarily harbors in weakened host trees (Thatcher and Pickard, 1964). However, D. frontalis populations also display regional outbreaks that can last from one to several years, kill large expanses of pine trees and transform forests (Clarke et al., 2016). One or two epidemics per decade have been common for the region (Birt, 2011). The population dynamics of D. frontalis are apparently governed by a nonlinear density-dependent feedback system with two locally stable equilibria (endemic and epidemic) separated by a region of positive feedback that produces an unstable equilibrium (escape threshold) (Martinson et al., 2013). When population abundance is near the escape threshold, even modest environmental effects on beetle survival and reproduction can produce a state change (e.g., endemic to epidemic). Factors that are candidates to produce such effects with D. frontalis include forest structure and silvicultural practices (Nowak et al., 2015; Asaro et al., 2017; Aoki et al., 2018), predation (Reeve, 1997; Weed et al., 2017), environmental effects on tree physiology (Lorio, 1986; Reeve et al., 1995; Lombardero et al., 2000a), active suppression by forest managers (Clarke and Billings, 2003; Billings, 2011), interactions involving mites and antagonistic fungi (Hofstetter et al., 2006a), the coldest night of the winter (Ungerer et al., 1999; Tran et al., 2007), and other features of weather (Reeve, 2018).
Over the past 25 years, impacts from this insect have been declining throughout the southern pine region, despite a simultaneous increase in pine habitat (Clarke et al., 2016; Asaro et al., 2017). A number of hypotheses have been put forth to explain this pattern, including changes to forest structure and host resistance from improved management and tree breeding programs, as well as climatological impacts from anthropogenic climate change (see Asaro et al., 2017). While a climatological explanation is plausible, there has not been a discernible link between climate and D. frontalis outbreaks in the South. However, most studies of climatological factors have focused on the positive influence of extreme climate events promoting outbreaks via their effect on host trees (Friedenberg et al., 2008; Asaro et al., 2017). For example, drought and/or high temperatures could weaken hosts and lead to outbreaks (McNichol et al., 2019). Alternatively, regional changes in climate could directly impact survival of D. frontalis, and in that manner alter the occurrence of local outbreaks (Ayres and Lombardero, 2000). Such influence of climate on population has already been seen at the northern extent of their distribution, where recent increases in minimum winter air temperatures have permitted an expansion of D. frontalis outbreaks into New Jersey, Long Island, and Connecticut (Lesk et al., 2017; Dodds et al., 2018), even as impacts within their historic southern range were declining. One possible explanation for the increase in outbreaks at the northern edge of their range and declining impacts in the South is that southern forests have become too warm for D. frontalis, even as northern forests have only recently become warm enough. This would be as expected under the hypothesis of climatic envelopes (Hijmans and Graham, 2006; Green et al., 2008), which predicts approximately symmetrical changes at the warmer and cooler distribution limits given approximately uniform climate warming. The envelope model, in various forms, underlies many forms of species distribution models (Pecchi et al., 2019), but has been difficult to test (Hao et al., 2019). One alternative hypothesis is that warmer is better for many ectotherms at both the warm and cool edges of their distributions (Frazier et al., 2006).
General circulation models predict a continuing rise in mean surface temperatures across most of the northern hemisphere (IPCC, 2013). This can result in less severe minimum winter temperatures (Easterling et al., 1997; Vose et al., 2005; Tran et al., 2007; Daly et al., 2012; Weed et al., 2013) as well as more intense and longer lasting heat waves (Easterling et al., 2000; Meehl and Tebaldi, 2004; Lyon et al., 2019). Some changes in thermal extremes can affect the distribution and abundance of biological populations (Pörtner, 2002; Haynes et al., 2014; Buckley and Huey, 2016; Lloret and Kitzberger, 2018).
Insects die differently from heat than from cold. Many insects, including D. frontalis, are freeze-intolerant (Duman et al., 1991) and have a discrete lower lethal temperature that corresponds to their supercooling point (the temperature at which fluids crystallize and cell membranes rupture). In D. frontalis, brief exposure to temperatures below the supercooling point ensure death, whereas sustained exposure to temperatures slightly above the supercooling point have little effect on survival (Lombardero et al., 2000b). Thus, the effects of cold on overwinter survival of wild populations can be realistically modeled based on the coldest night of the winter (Tran et al., 2007); duration of exposure matters relatively little (Lombardero et al., 2000b). However, when insects die from heat, mechanisms include destabilization of membranes and proteins, increase in reactive oxygen species, as well as disruption of oxygen delivery, water budgets, and energy balance (McCue and De Los Santos, 2013). Depending on the mechanism, the duration of heat exposure required to produce mortality might vary from hours to days, and exact cause of death is likely to depend upon the intensity and duration of heat exposure (Rezende et al., 2014).
We tested the hypothesis that the historic range in the southeastern United States is becoming too hot for D. frontalis by (1) experimentally measuring effects of heat exposure on insect survival, (2) characterizing the thermal environment of D. frontalis within the inner bark of host trees, (3) estimating the historical frequency of potentially lethal heat waves in the historic range of D. frontalis, and (4) testing whether the intensity or duration of heat waves has been increasing during recent decades.
Section snippets
Acute high temperature exposure
Tests of mortality from high temperature exposure required exposing larvae to bouts of high temperature in situ. This is not easily accomplished in the field because southern pine beetle larvae inhabit the inner bark (phloem) of trees. However, it was possible to conduct laboratory experiments with beetle-infested bark from trees, and with sections of infested bole from felled trees. In July 2011, we removed portions of bark from 12 infested pitch pine trees within a southern pine beetle
Results
There were no effects on survival of D. frontalis from acute exposure (one day) to a maximum daily temperature of either 37 °C or 42 °C (Table 1). By comparison, Beal (1933), who studied sun-warmed logs, reported some mortality of D. frontalis with phloem temperatures of 38 °C and high mortality at 43 °C. Thus, the upper lethal temperature for 50% mortality of D. frontalis from a one-day exposure is no less than 38 °C and is probably >40 °C. We found no effects of chronic high temperature
Discussion
The reduced abundance of D. frontalis in southern forests is not due to direct mortality from an increase in the maximum summer temperatures. Rarely, if ever, have air temperatures approached lethal levels for D. frontalis over 80 years of daily records for our study region. Moreover, there has been no increase in yearly maximum temperatures, nor any significant change in the duration or severity of sequential warm days (heat waves). Other studies have similarly reported that maximum
Funding
This research was financially supported by NRI/AFRI 2009-65,104-05,731 and a cooperative agreement with the Southern Research Station.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank the New Jersey Department of Environmental Protection and officials of the Homochitto National Forests for help in acquiring resources. Thanks also to Ken Clark, John Dighton, JoAnne Barrett, Matt Cloud, and Erich Vallery for logistical and field support.
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